Flystrike in New Zealand: an Overview Based on a 16-Year Study

Veterinary Parasitology 137 (2006) 333–344 www.elsevier.com/locate/vetpar

Flystrike in New Zealand: An overview based on a 16-year study, following the introduction and dispersal of the Australian sheep blowﬂy, Lucilia cuprina Wiedemann (Diptera: Calliphoridae)

A.C.G. Heath a,*, D.M. Bishop b

a AgResearch, Wallaceville Animal Research Centre, P.O. Box 40063, Upper Hutt, New Zealand b 244 Blue Mountains Rd., Upper Hutt, New Zealand

Received 14 September 2005; received in revised form 19 December 2005; accepted 10 January 2006

Abstract

A summary and analysis have been carried out on data from over 6000 instances of flystrike in sheep in NZ, over a 16-year period, using a self-referral system where farmers submitted larvae and related information. The study covered a period of establishment and subsequent countrywide spread of the exotic blowfly, Lucilia cuprina. Comparisons are drawn between flystrike as it was perceived by surveys carried out before the 1940s, and the current situation with L. cuprina as an added major impediment. Briefly, the main differences are an increase in the prevalence of flystrike, changes in the representation and relative influence of individual primary blowfly species, an extension of the flystrike ‘season’, and an apparent increase in the importance of footrot as a factor predisposing to flystrike. Otherwise, flystrike is still primarily a disease of ewe lambs that are struck predominantly around the tail and perineum, mainly because of faecal staining. # 2006 Elsevier B.V. All rights reserved.

Keywords: Flystrike; Lucilia cuprina; Epidemiology; New Zealand

1. Introduction and welfare concerns in other countries (Hall and Wall, 1995). Flystrike is an extension of the carrion- Flystrike is not only a perennial problem for the feeding habits of a few species of Calliphoridae New Zealand (NZ) sheep farmer, with estimated (Zumpt, 1965), wherein gravid female blowflies are annual losses a decade ago of at least $30–40 million attracted to sheep by a variety of cues, predominantly (Heath and Bishop, 1995), but also causes production olfactory, and stimulated to deposit eggs or live larvae under the influence of another set of cues (Hall and Wall, 1995). There are numerous pathological effects * Corresponding authors. Tel.: +64 4 529 0436; fax: +64 4 529 0380. of flystrike resulting from both mechanical and E-mail address: [email protected] (A.C.G. Heath). chemical attack by the feeding activity of maggots.

Flystrike was officially reported as a problem in NZ Heath et al. (1983) emphasised correct dipping in the 1890s (Heath, 1994), although the initiating flies procedures and the value of monitoring fly activity, were first noticed in the 1870s (Hutton, 1901; Gilruth, and were an attempt to satisfy the need for information 1907) and by 1901 some apparently were established appropriate to farmers but, in hindsight, did not have nationwide (Hutton, 1901). Flystrike was severe the benefit of a full and current understanding of the enough as a problem by the 1920s for a survey of problem. The current study was intended to rectify this its prevalence and distribution to be undertaken situation, at least in part. (Miller, 1921) and parasitoid wasps imported as a Part way into the present study, in 1988, L. cuprina potential control measure but they had little apparent was found in NZ (Heath et al., 1991; Holloway, 1991) effect (Heath and Bishop, 1989). Since then a small but its distribution was incompletely known. This number of studies have contributed towards further provided a rare opportunity to chart the progress of a understanding of the epidemiology of flystrike in NZ, relatively recently introduced species, and also with nationwide (Miller, 1939) and locality studies suggested a possible reason for the changed percep- (Macfarlane, 1941; Dymock et al., 1991) together with tions about flystrike that had been reported by farmers an economic survey (Tenquist and Wright, 1976). about 5–6 years earlier. The short term (1 year at most) or localised nature of these studies precluded any assessment of national and annual trends in flystrike prevalence and onset, as 2. Materials and methods well as any changes in the blowfly fauna, information which is relevant for helping to understand and The principal basis of this study was self-referral of manage flystrike. In addition, previous studies, with samples of blowfly larvae collected by farmers from the exception of Dymock et al. (1991), that was based sheep, or other livestock species they encountered solely on fly trapping, dealt with a primary flystrike with flystrike. Data were recorded that were pertinent fauna that comprised just three species of blowflies to each host that was struck, including its age, sex and (Lucilia sericata, Calliphora stygia, Chrysomya factors that might have predisposed to the strike. rufifacies), and lacked Lucilia cuprina, the Australian About 50 farmers stayed with the project from the sheep blowfly, which only became apparent in NZ in beginning, having been initially chosen as a core the 1980s. monitor group. Other farmers were recruited as the Between 1982 and 1983, reports were received project grew, and many were self-selected having from farmers who were convinced that both the decided to participate once they were made aware of prevalence and seasonal duration of flystrike had the study. In all 1009 farmers participated at some time increased from what had been previously experienced. during the duration of the study. In the few studies carried out between 1920 and 1976 Farmers were provided with collection pots and flystrike was recorded as an annual nuisance but given clear instructions on sampling and recording accepted as a manageable problem. There was a procedures, and provided with a standardised record- relatively well-defined ‘‘season’’ that extended from ing form. They were also kept appraised of results in November to February (Heath, 1986a) with flystrike of regular newsletters in an attempt to maintain their little concern outside those months, if it occurred at all. interest and support in the project. Farmers were To account for the apparently altered circumstances provided with additional collection pots as these were reported in the 1980s there was speculation that long- requested. term climate change may have been influential (Heath, 1986b) and there were reports of a ‘new fly’ but 2.1. Larval samples nothing was submitted to us that caused alarm. We concluded that the usual pattern of flystrike was just Briefly, farmers were asked to submit samples of experiencing a brief, temporary perturbation. Despite larvae from active flystrike lesions on their sheep. this, the nature of continuing farmer concerns and Larvae were sent to the laboratory by post after being questions indicated that there was an absence of up-to- collected into a container partly filled with expanded date information on flystrike. Guidelines produced by biotite (Vermiculite1) that had been pre-delivered to A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 335 farmers. Samples were usually received by us within 1 when they took samples, and they could add others or 2 days of collection, and any that farmers could not not on the list. send immediately were stored at 4 8C for up to 3 days before posting without apparent ill-effects to larvae. A 2.3. Host data recording form (see details below) included with the pre-delivered containers accompanied each sample, 2.3.1. Sex and age the expectation being that submitters would complete For sorting data on age and sex distribution of as many of the sections as they were able. strikes in sheep the categories lambs, 12 month to two A sub-sample of larvae was taken from each tooth (12 mth–2 th) and older than two tooth (>2 th) sample when received, killed in boiling water, and were used, with Belschner (1976) as a guide. stored in 70% ethanol. These served as voucher specimens and as a means of identification should 2.4. Topography of strikes adult flies not be bred from the remaining larvae. Larvae were identified using descriptions in Dear When analysing the strike location sketches supplied (1986) and Holloway (1991).Iflarvaehaddiedand by farmers, it was found convenient to group data deteriorated during postage, it was sometimes still according to whereabouts in four anatomically distinct possible to identify them to species. The exception ‘quadrants’, the ‘Head’, ‘Flank’, ‘Rear’ and ‘Abdom- was some samples of Lucilia larvae where only a inal’ strikes most commonly occurred. Where strike generic description was possible, hence these are lesions crossed quadrant boundaries they were scored in presented as Lucilia spp. each quadrant in which they occurred. The remaining live larvae in each sample were placed in a container of rearing medium in an 2.5. Geographic distribution of flystrike incubator at 26 8C to mature and pupate. Puparia from which flies had not enclosed after an expected interval Source data were sorted into geographic regions (usually 10–14 days), were set aside to await the using the boundaries and locality code system emergence of any parasitoid wasps that might be proposed by Crosby et al. (1976, 1998). A map present (Heath and Bishop, 1989; Bishop et al., 1996). (Fig. 1) used with permission of the Fauna of New Adult flies were identified using descriptions in Dear Zealand series (Landcare Research), shows these (1986) and Bishop (1991). regions and their codes. Each district is referred to in On numerous occasions completed recording forms full with its code in parentheses at first use, and were submitted, but no sample of larvae. Any thereafter only full names are used. information thus provided relating to host age and sex, position of strike and factors predisposing to 2.6. Fly trapping strike, were incorporated into the study where appropriate. Once it became apparent that L. cuprina was in the South Island, flytraps of modified Western Australian 2.2. Recording form design (Cole, 1996) baited with thawed sheep’s liver submerged in 10% sodium sulphide solution, were The recording form supplied to farmers requested deployed. Sites on farms and schools at the margins of their name and address, date of collection of larvae, the last reported finding of L. cuprina were selected in number of samples submitted, breed, age and sex of order to anticipate further extensions of its range. host animal. Two diagrams of a sheep (rear and Either six or eight traps were used each time, set-up on dorsal views) were supplied on which the approx- the chosen trapping sites within a geographic area that imate extent of the flystrike lesion(s) could be would typically cover about 30–50 km2, and cleared sketched. A list of factors and operations present or weekly. Initially the traps were shifted to new sites occurring at the time (shearing, docking, footrot, once each year or ‘season’, but if it became apparent crutching, tick bites, prolapse, scouring) was that L. cuprina was extending its range more rapidly provided for farmers to choose from and record than expected, then the traps would be moved to new 336 A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344

2.7. Seasonal data

The terms ‘season’ or ‘ﬂystrike season’ are colloquial and refer to the period from when ﬂystrike becomes noticeable in the ewes and new crop of lambs each year (usually around October) until its obvious decline (around March or April in the next year) when its prevalence is less. Thus, portions of two calendar years are bridged, and most of two seasons (spring and summer) incorporated.

2.8. Intentions questionnaire

Once, in 1999, a questionnaire was sent to 356 farmers who had been regular submitters of larval samples. Participants were asked to nominate the month in which they encountered most instances of flystrike, as well as months in which they undertook specified farming operations during which they discovered flystrike.

2.9. Statistical analysis

This was not designed to be a controlled study and bias is an unavoidable consequence of the self- referral, self-selection methodology used. This made much of the data uninterpretable in terms of signiﬁcance of possible contributory effects. However, where appropriate a Chi-square analysis of proportions was carried out (L. Morrison, Personal communication).

3. Results

Unless otherwise speciﬁed, the data presented here encompass the years 1984–2000, and represent 16 years or ‘seasons’.

3.1. Monthly and annual distribution of samples Fig. 1. Map showing area codes used, and ﬁrst recorded year for L. cuprina in each region. See text for details. More North Island samples were received in March (22.4%) than in any other month, closely followed by sites within a year or ‘season’. The use of schools was February (22.0%), with 61.8% overall submitted in both a part of the 1992–1994 science education January to March inclusive. In the South Island most Flytrack initiative (Bishop et al., 1992) and later, samples were received in January (21.4%), with exploitation of residual interest by schools in that 60.6% overall submitted in January to March programme. inclusive. A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 337

Samples were received every year in the North Table 2 Island for the duration of the study (n = 16 ‘seasons’), Distribution of samples (number and percentage) by age and sex of sheep, as well as where these were unspecified with a range of 65 (1984–1985) to 459 (1989–1990) samples. In the South Island samples were first Sex N % Age N % submitted in 1986–1987, giving a range over the study Female 3578 54.5 Lamb 2987 45.5 of 3 (1987–1988) to 244 (1998–1999) samples over Male 865 13.2 12 mth–2 th 837 12.7 Castrate 476 7.2 >2 th 1484 22.6 n = 14 ‘seasons’. Totala 4919 5308 3.2. Geographic distribution of samples Unspecified 1650 25.1 Unspecified 1261 19.2 Totalb 6569 100.0 6569 100.0 An analysis of the 13 possible North Island regional a Where sex and age specified. sources of samples showed that nearly 54.0% came b ‘Forms only’ and ‘no samples’ are included in this total, which from only three regions, i.e. Gisborne (GB), Wanganui accounts for discrepancy between totals in these data and those in (WI) and Waikato (WO) in descending order of Table 1. sample quantity, with Wellington (WN) and Hawkes Bay (HB) next. In the South Island 56.2% came from (6.0%) and Corriedale (5.5%) including their crosses. Mid Canterbury (MC), North Canterbury (NC) and The remainder of records included representatives of Marlborough (MB), in that order, with Nelson (NN) nearly every breed present in NZ. In the national flock and South Canterbury (SC) next. No samples were the five numerically most common breeds are received at all from Stewart Is (SI) or Fiordland (FD), Romney, Coopworth, Perendale, Corriedale and leaving a total of a possible 14 South Island regional Merino, in that order (Anon, 1994). sources of larvae (Table 1). 3.5. Topographic distribution of flystrike lesions 3.3. Age and sex distribution of samples of larvae from flystruck sheep 3.5.1. Distribution by sex There were 5396 records for topographic distribu- On some occasions completed forms were sub- tion of flystrike lesions amongst sheep where the sex mitted, but without accompanying larvae and these data was specified, with the rear quadrant attracting most were incorporated where appropriate, e.g. Table 2. strikes (n = 3713; 68.8%), followed by the flank Samples of larvae were most frequently obtained (25.6%), abdomen (3.6%) and head (1.9%). These from female sheep (3578/4919; 72.7%) and the lamb rankings were consistent among females, males and age class (2987/5308; 56.3%). castrates.

3.4. Breeds of sheep 3.5.2. Distribution by age There were 5745 records for topographic distribu- Analysis of 4385 records relating sheep breed and tion of flystrike amongst sheep where the age was flystrike occurrence showed that Romney and Romney specified, with the rear quadrant attracting most strikes cross predominated (55.1% of records), followed by (n = 3978; 69.2%), followed by the flank (25.3%), Coopworth (10.3%), Merino (8.2%), Perendale abdomen (3.4%) and head (2.0%).

Table 1 Monthly totals of samples of larvae received from both North and South Island farms throughout the study Island Months Totals January February March April May June July August September October November December North 803 1015 1035 499 170 15 4 4 15 135 373 565 4613 South 344 321 308 178 49 4 3 7 5 27 119 241 1606 Totals 1147 1336 1343 677 219 19 7 11 20 162 492 806 6219 338 A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344

The proportions of flystrike distribution in the age 3.8. Non-ovine hosts for flystrike groups only were compared using Chi-square. Lambs had significantly more strikes on the rear quadrant but A total of 50 samples of larvae came from hosts fewer on the flank than expected, while there were other than sheep, with goats (40 samples), cattle (9) fewer strikes on the rear quadrant of 12 mth–2 th sheep and dog (1) represented. For the goats, flies were but more on the flank than expected (Chi- reared out from larvae on 26 occasions, with L. square = 129.4; d.f. 6; p < 0.01). cuprina (six occasions), L. sericata (4) and Ch. rufifacies (2) each represented in monospecific strikes 3.6. Factors predisposing to flystrike and a further eight strikes comprising mixtures of those three species, together with C. stygia. Uni- Most submitters ignored this section of the record dentified Lucilia spp. were reared out on six occasions. sheet, and as a consequence there were only 874 The strikes in goats were almost exclusively in the records, with ‘scouring’ and ‘dags’ combined feet. Strikes in cattle were either on faecal material or predominating (68.9%) followed by footrot (8.2%) scabs. prolapse (2.9%) and dermatophilosis (2.3%). Of the remainder, unspecified ‘other’ causes totalled 3.9. Regional and seasonal distribution 15.6%. of strike flies

3.7. Blowfly fauna Perhaps not unexpectedly, each species of strike fly occurred most frequently in regions that were the Throughout the study 6219 samples of larvae were source of the greatest number of samples of larvae. submitted, and those in 6047 samples were identifiable to genus or species. Of these, 3000 were monospecific 3.9.1. L. cuprina strikes comprising 48.3% (1449/3000) L. cuprina, By 1989, this species occurred in samples from all 21.5% L. sericata, 23.6% C. stygia and 6.6% Ch. North Island localities depicted in Fig. 1, although it rufifacies. In the 3219 multispecies’ strikes, 2205 was still extending its range into some previously contained L. cuprina, 2336 contained L. sericata, 1538 unaffected farms within those regions up to 1999, contained C. stygia, and 206 contained Ch. rufifacies. especially in Wanganui, Rangitikei (RI) and Taranaki Flies that could only be identified as Lucilia spp. (TK). Before 1988, we have no records for L. cuprina occurred alone in 116 strikes and with other species on in Northland (ND), Taranaki or Wairarapa (WA). The 112 occasions. earliest confirmed record for L. cuprina came after In multispecies’ mixes of primary flies, pair inspection of preserved larval material from Wairoa combinations were the most commonly encountered (GB) obtained in 1984. (2145/3047), with an L. cuprina/L. sericata mix being In the North Island, L. cuprina was bred out from most frequently reared out of samples (1129/3047) samples of larvae submitted each month, except those and L. sericata/C. stygia next (550/3047). All four received in July and August. It was most common species of primary flies sometimes occurred together, between November in 1 year through to May in the being reared out of samples of larvae on 21/3047 next, with >100 records of its occurrence in samples occasions. of larvae in each month over that period. In the South In 26 samples, flies were bred out that are not Island, L. cuprina was not taken from samples of normally regarded as part of the primary flystrike larvae between June and September. Its most common fauna. These were C. vicina in seven mixed strikes months of occurrence (>100 records per month) were (and once by itself), C. hilli in three mixed strikes, C. January to April inclusive, with a first appearance in quadrimaculata in two mixed strikes (and once by October. itself) and Xenocalliphora hortona in three mixed There are no records of L. cuprina in the South strikes. Two species of Muscidae occurred in mixed Island before the 1990, but in that year it was found to strikes, Musca domestica in six and Hydrotaea be present in Kaikoura (KA) and Marlborough (Fig. 1) rostrata in seven. and then, in 1991 the species was found in North A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 339

Canterbury and Mid Canterbury and, in 1994, the 3.9.3. C. stygia Marlborough Sounds (SD). It was not until 1995 that This species was reared out from 1697 samples L. cuprina was found in South Canterbury. By 1996, submitted from all North Island localities and 644 L. cuprina occurred in only six of 14 South Island from the South Island. C. stygia occurred most localities that samples were submitted from. frequently in strikes in Gisborne (19.8% of all Most submissions came from Marlborough followed samples), Wanganui and Wellington (12.7% each) byMidCanterburyandNorthCanterbury,then and Wairarapa (10.8%) in the North Island. In the Kaikoura, South Canterbury and Nelson. In 1997, L. South Island the proportions were: North Canterbury cuprina was discovered in Dunedin (DN) and in (21.9% of all samples), Marlborough (14.1%), Mid Central Otago (CO) in 1998. By 1999, L. cuprina Canterbury (11.2%) and Nelson (10.2%). was being detected in the MacKenzie Basin (MK), C. stygia was present in samples every month of the Otago Lakes region (OL), and Southland (SL), as year in both islands. The period of October in 1 year to well as Westland (WD). There are no records from March in the next was the peak flystrike season for C. the Buller (BR) region, although samples were stygia in the North Island with >100 records each of received from there only in the 1989–1990 and those months. In the South Island, only December, 1991–1992 seasons. January and February each had >100 records of C. With the exception of the first Dunedin record, that stygia, although November and March each had >70 was obtained through trapping, all new regional records. records for L. cuprina in the South Island came via larval samples from flystruck sheep. Trapping was 3.9.4. Ch. rufifacies useful, however, for monitoring range extension of L. This species was principally recovered from cuprina within regions. This was particularly apparent samples of larvae submitted from the North Island, in Mid Canterbury and South Canterbury where a total there being only two records for the South Island of 29 trapping sites were employed (12 in Mid (from adults trapped in Nelson and North Canterbury). Canterbury during 1994–1995 and 17 in South The seasonal activity of Ch. rufifacies was at its peak Canterbury during 1995–1996) and L. cuprina was from January to April inclusive when ca. 98% of detected progressively as it moved southwards and samples containing this species were received (444/ inland into previously unaffected localities. 454), with additional, occasional records in May, August and December only. Peak flystrike activity 3.9.2. L. sericata (>100 cases per month) occurred in February and This species was reared from samples submitted March. from all North Island and South Island localities in Ch. rufifacies was most common in the Gisborne the survey. It occurred most commonly in samples and Waikato regions, being present in 19.4% of from Wanganui (25.8% of all L. sericata records for samples from each of them. The northern North Island the North Island), followed by Gisborne (24.7%), preference for this species was further emphasised with Wairarapa (13.1%) and Hawkes Bay (11.5%) with the Bay of Plenty (BP) and Northland regions next. In the South Island, L. sericata occurred having it present in 11.0% and 9.7% of samples, most frequently in samples from Mid Canterbury respectively, and Auckland (AK) 9.5%. Collectively, (24.2%), North Canterbury (22.7%) and Marlbor- these regions accounted for 68.9% of all Ch. rufifacies ough (14.7%). records. L. sericata was reared out of samples received over 10 months of the year in the North Island (June and 3.10. Intentions questionnaire July excepted). There were no July, August or September records in the South Island. Peak partici- A total of 30 farmers from the North Island and pation in strikes in the North Island occurred between 37 from the South Island responded to the ques- November in 1 year and April in the next, and between tionnaire. Not all questions were answered, leaving the December and April in the South Island (>100 records replies from only 62 respondents usable in respect of each month in each instance). what motivated submission of samples of larvae. In all, 340 A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344

48/62 indicated they regularly monitored sheep, with For example, about 75% of farmers who responded to the remainder only finding affected sheep during a questionnaire on how they encountered struck sheep routine farming operations, such as docking, crutching/ reported they did so while looking specifically for dagging, drenching, etc. North Island farmers reported flystrike. Some districts in the present study may also January, February and December the months in which have benefited from assiduous efforts on the part of flystrike was most frequently encountered, although all veterinarians or consultants to encourage farmer months except June and July were mentioned. South participation following field days held by us, or as a Island farmers reported January, December, November result of our research activity in an area. Despite these and March as months when flystrike was most limitations and possible biases, the study provided frequently encountered, although all months except data for a useful summation of the major components June, July and August were mentioned. of the flystrike problem in NZ, and produced a better profile than would shorter or less extensive surveys.

4. Discussion 4.2. Review of earlier studies

4.1. Limitations of the study Early records of flystrike showed it to be more common in lambs and hoggets than in other age The study reported here was not a systematic groups, with ewes outnumbering wethers and rams, sampling programme, with a specified set of farms, andwithdampanddirtywoolpredisposingfactors sampled at set intervals, but its duration, sample size (Miller, 1921, 1922). Most strikes were found in the and coverage provide a basis for a generalised, crutch/breech/rump/tail region and in a nationwide descriptive view of flystrike epidemiology in NZ. survey of 155 cases of flystrike (Miller, 1939), 67.3% In the initial stages of this investigation (1984– of strikes were at the rear end of the sheep and 20.2% 1986) a small number of properties in the Hawkes Bay on the neck and ‘body’, with so-called ‘clean’ sheep and Wellington districts only were involved. These struck about the shoulder. In a Marlborough region farms had been selected because of a history of high survey of 1352 sheep (Macfarlane, 1938, 1941) prevalence of flystrike in flocks. In subsequent years 41.9% had back strike, but breech/crutch strike there was a nationwide publicity campaign that asked predominated (53.7% of strikes) with urine and for more farmers to submit samples and a greater faecal soiling the main source of attraction for flies number eventually participated. and the predominance of fine-wooled sheep with There are limitations to the self-referral, self- crutch wrinkles in Macfarlane’s (1941) sample may selection systems employed here (used also by Miller, have accounted for the high prevalence of back 1921, 1922), the principal one being the number of strike, a condition that is common in the Australian uncontrolled variables. For instance it is unlikely that a merino (Wardhaugh and Morton, 1990). Body strike fully representative sample of the species mix of was associated with periods of warm, heavy rain larvae from each sheep would be obtained. Larvae followed by dry periods, but bacterial conditions would have been collected at any stage during the such as fleece rot were not a regular accompaniment progress of a strike but it is more likely that advanced (Macfarlane, 1941). strikes (>24 h old) would be the source of most The species of flies reared out from strikes in early submissions. These are more easily detected than early studies (Macfarlane, 1941; Miller, 1921, 1939) were strikes because they are associated with wool-stain, mainly C. stygia (known then as Pollenia stygia or C. odour and distinctive host behaviour. Another draw- laemica) which appeared in 49% to >90% of strikes, back to the methodology is that a representative with L. sericata next in 5–46.3% of strikes A number demographic sample of all sheep flystruck at a of other species of calliphorid and muscid flies were particular time or locality is unlikely to be achieved, reared out from strikes including Ch. rufifacies. This meaning that valid year-to-year comparisons are species was first recorded in the North Island by Miller precluded. Furthermore, some farmers can be more (1922), with a possible but unconfirmed record in an enthusiastic about participation in a study than others. earlier study (Miller, 1921). Ch. rufifacies was later A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 341 found in 1.4% of strikes (Miller, 1939) in the North 4.4. The current face of flystrike in NZ: the Island and occurred, but rarely, in Marlborough in the influence of L. cuprina South Island (Macfarlane, 1941). The seasonality of flystrike was incompletely So what has changed since the 1920s and 1930s? determined in early surveys as they did not cover The biggest single influence on the epidemiology the complete calendar year and measures of variation and natural history of flystrike in NZ has been the in prevalence of flystrike between districts were not establishment of the Australian sheep blowfly L. comprehensive. cuprina. Molecular genetics studies suggest this species was introduced from Australia (Gleeson, 4.3. Findings of the current study 1996). Of the two subspecies recognised in Australia (Waterhouse and Paramonov, 1950; Norris, 1990) Comparisons between the foregoing historical data New Zealand has L. c. dorsalis, the more common of and those in the present study can only be done with the two (Bishop, 1995). caution. Differences in sample size, as well as L. cuprina is pre-eminent as a primary strike fly in duration and extent of the studies need to be Australia (Shanahan, 1965) using live sheep for considered, together with a different blowfly faunal population maintenance in the arid zone, with some mix, a changed sheep population and shearing breeding also occurring in carrion in more temperate patterns, and the use of an entirely different set of areas (Anderson et al., 1988), in rubbish tips in New anthelmintic and insecticidal materials in sheep South Wales (McKenzie, 1984) and household rubbish husbandry. in Brisbane (Rice, 1986). The species is principally Despite these constraints, lambs, and particularly involved in breech strikes in Merino ewes, with body females, still remain the more frequently flystruck age strike troublesome in years of excessive rainfall during and sex combination in the NZ sheep population. The the warmer months (Shanahan, 1965). In NZ, L. rear end of the body still most at risk, mainly as a cuprina is almost exclusively associated with sheep result of soiling from faeces. There is no conflict here (Gleeson and Heath, 1997) some carrion (Heath and with historical data. The predominance of female Appleton, 2000) but rarely in rubbish tips (Dymock hosts is most likely to be due to their greater and Forgie, 1993; Gleeson and Heath, 1997). proportional representation in the national sheep Control of L. cuprina has always been problematic, flock. Breeding ewes represented 68.2% of the as indeed it is with all myiasis-causing flies (Hall and 47.394 Â 106 sheep in New Zealand in 1999 (Anon, Wall, 1995) but its resistance to organophosphate dip 2002) with lamb births increasing the number of chemicals, a characteristic accompanying the NZ females each year, for a short period, until culling strain(s) of L. cuprina, has not helped (Gleeson et al., supervenes. Similarly, representation on the basis of 1994; Wilson and Heath, 1994). Sole reliance on breedplacedRomneyandRomneycrossasfirst insecticides has also increased the risk of erection of ranked, which is their position in the national flock non-tariff trade barriers because of insecticide (Anon, 1994). However, our findings indicate that residues in wool (Edwards, 1997). These concerns Merino and Merino cross sheep may be at slightly and the multi-factorial nature of flystrike, lead to the greaterrisktoflystrike(rankedthirdinthestudy)than development and promotion of an integrated manage- their representation in the national flock (ranked fifth) ment programme in NZ (Cole and Heath, 1999). It was would attest (Anon, 1994). designed to use specialist forages (Leathwick and Footrot appears as a considerably more influential Heath, 2001), removal of fly breeding sources (Heath predisposing factor in flystrike in the present study and Appleton, 2000), fly trapping and activity than in previous reports. Macfarlane (1941) recorded monitoring (Heath and Leathwick, 2001), parasitoids around 1.3% in flocks studied, whereas our data show (Bishop et al., 1996) and targeted insecticide use (Cole 8.2%. This difference is not readily explained, but the and Heath, 1999). The programme was successful and figure serves to highlight the role of flystrike of feet in cost-effective, but transference of the technologies so-called covert strikes (Wardhaugh and Dallwitz, required considerable extension work with farmers. 1984). However, its attractiveness was in its immediate 342 A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 applicability, as new technologies, e.g. Heinrich et al. Overall, range expansion of L. cuprina was (2002) were far from complete. considered more likely to be through transport of The discovery of L. cuprina in NZ in 1988 infested sheep than by fly dispersal (Gleeson and Heath, (Holloway, 1991) was consequent upon its likely 1997) although the moderate rate at which L. cuprina introduction in the late 1970s (Heath et al., 1991)a extended its range within the South Island from 1990 to supposition based on three pieces of evidence: (1) L. 1997 would not preclude self-introduction. cuprina was absent in insect collections prior to 1960 Despite being predominant in breech and body (Dear, 1986). (2) There was no reported consistent strikes in Australia (Wardhaugh and Morton, 1990), L. change in flystrike prevalence and severity before the cuprina is not common in body strikes (shoulders and 1980s (Heath and Bishop, Personal observation) withers) in NZ, although it is often anecdotally although L. cuprina was present in 1984 (this study). associated thus by farmers (Heath and Bishop, (3) Despite L. cuprina being throughout the North unpublished). Merinos comprised 8.2% of breeds Island by 1989, it had a discontinuous distribution and sampled in the current study, but neither fleece rot nor continued to progressively invade previously unaf- dermatophilosis, conditions that frequently predispose fected farms (Heath and Bishop, 1995). to body strike in Australia (Wardhaugh and Morton, L. cuprina was not present in the small number of 1990) were identified in our study as major samples received between 1984 and 1988 from contributing factors to flystrike. On one occasion, Wairarapa, Taranaki or Northland, and may not have when fleece rot appeared to be a precipitating factor reached these regions. Alternatively the small number for body strike in >100 sheep in a South Island flock, of samples could have precluded its detection. after heavy rainfall, only L. sericata was bred out. There was no evidence of L. cuprina in the South Before L. cuprina was a feature of the NZ flystrike Island before 1989 despite a total of 124 samples of fauna, most strikes sampled by early workers identified larvae being received, beginning in 1986 (this study). C. stygia as the predominant primary fly, occurring in At the time of its first detection in the South Island in >50% of samples (Miller, 1922, 1939; Macfarlane, 1990, L. cuprina was present in both Kaikoura and 1941; Heath, 1986a). The current study obtained that Marlborough. Continued sampling and then deploy- species from 12.0% of all samples of larvae submitted, ment of monitor traps from1993 onwards, demon- with L. cuprina in the principal role as flystrike initiator strated the gradual expansion of its range southwards in 60.4% of all samples. L. sericata was represented in and westwards over the 8 or 9 years following its first samples at proportions comparable with those found in detection (Bishop et al., 1991; Bishop and Heath, earlier studies but, on the other hand, Ch. rufifacies 1997; this study). This was taken as evidence for a appears to have increased its representation in strikes relatively recent introduction. Between 1991 and 1995 compared with historical data. there was no apparent expansion of range beyond A consequence of L. cuprina strike initiation could Kaikoura, Marlborough, Marlborough Sounds, North be that species composition in samples of larvae Canterbury and Mid Canterbury, but there seemed to submitted for identification are biased towards L. be a period of consolidation within Mid Canterbury. cuprina if taken early in strike establishment, and This was detected partly by trapping, partly through towards other species if intervention (sample collec- flystrike larval samples, and also farmers noticing tion) in the strike is later in the establishment phase. flystrike on what they considered low risk (i.e. ‘clean’) Collection of larvae from flystrike lesions at a late sheep, until L. cuprina eventually showed up in South stage could mean that predation by Ch. rufifacies Canterbury. Movement then seemed to be via the reduced the prevalence of other species that may have eastern coastal strip to Dunedin by 1997, then inland originally been present. This species is rare in the South to Central Otago by 1998. By 1999, L. cuprina Island, and was not taken from samples of larvae, there had completed its invasion of nearly all the South being only two records throughout the entire study Island, being found in Mackenzie, Otago Lakes and (South Canterbury and Nelson), and those from trapped Southland. This distribution represents the southern- adult specimens. It may have once been more common, most extension of the range of L. cuprina in the as Dear (1986) recorded material from Nelson, Southern Hemisphere. Marlborough Sounds and Kaikoura. Dear (1986) also A.C.G. Heath, D.M. Bishop / Veterinary Parasitology 137 (2006) 333–344 343 comments that Ch. rufifacies is unable to strike sheep Anon, 1994. New Zealand Sheep and their Wool, 5th ed. Wools of without prior infestation by primary invaders. However, New Zealand, Wellington, p. 64. Anon, 2002. New Zealand Official Yearbook, 103rd ed. Statistics the frequency with which we encountered Ch. rufifacies New Zealand, Auckland, p. 627. as the sole species in larval samples (6.9% of single Baumgartner, D.L., 1993. Review of Chrysomya rufifacies (Diptera: species’ samples), and where there was no clear Calliphoridae). J. Med. Entomol. 30, 338–352. evidence of other species having been eaten by this Belschner, H.G., 1976. Sheep Management and Diseases, 10th ed. facultative predator, lead us to conclude that it is able to Angus and Robertson, London, p. 838. Bishop, D.M., 1991. Variations in numbers of occipital setae for two initiate strikes. This role is supported by evidence from species of Lucilia (Diptera: Calliphoridae) in New Zealand. N. studies in other countries (Baumgartner, 1993). Z. Entomol. 14, 28–31. Bishop, D.M., 1995. Subspecies of the Australian green blowfly (Lucilia cuprina) recorded in New Zealand. N. Z. Vet. J. 43, 5. Conclusions 164–165. Bishop, D.M., Cole, D.J.W., Heath, A.C.G., 1992. Flytrack, the development and implementation of an idea. In: Proceedings of Flystrike has been a serious production-limiting the 41st Annual Conference of Entomological Society, New disease for NZ sheep farmers for more than a century. Zealand, May, p. 4. Its severity has increased in recent years for a variety Bishop, D.M., Heath, A.C.G., 1997. The impact of the Australian of reasons, some related to changes in farming practice green blowfly (Lucilia cuprina) on flystrike in New Zealand (Abstract). N. Z. J. Zool. 24, 295–296. and sheep densities, but principally because another Bishop, D.M., Heath, A.C.G., Cole, D.J.W., 1991. The Australian blowfly species has been added to the flystrike- green blowfly strikes again (Abstract). N. Z. J. Zool. 18, 88. initiating fauna. Despite the advent of efficacious and Bishop, D.M., Heath, A.C.G., Haack, N.A., 1996. Distribution, persistent insecticides, flystrike continues to be an prevalence and host associations of Hymenoptera parasitic on intractable problem. Calliphoridae occurring in flystrike in New Zealand. Med. Vet. Entomol. 10, 365–370. Cole, D.J.W., 1996. A further modification of the West Australian fly trap for blowfly studies. N. Z. Entomol. 19, 87–90. Acknowledgements Cole, D.J.W., Heath, A.C.G., 1999. Progress towards the development and adoption of integrated management systems against We thank all the farmers who were sufficiently flystrike and lice in sheep. Proc. N. Z. Grassld. Ass. 61, 37–42. Crosby, T.K., Dugdale, J.S., Watt, J.C., 1976. Recording specimen interested in the progress of our research to submit localities in New Zealand: an arbitrary system of areas and codes samples of blowfly larvae, sometimes the interest being defined. N. Z. J. Zool. 3, 69 +map. over many years. Grateful acknowledgement goes also Crosby, T.K., Dugdale, J.S., Watt, J.C., 1998. Area codes for to the many schoolchildren (and their teachers) and recording specimen localities in the New Zealand subregion. farmers who maintained flytraps during different N. Z. J. Zool. 25, 175–183. Dear, J.P., 1986. Calliphoridae (Insecta: Diptera). Fauna N. Z. 8 86 phases of this study. Finally we thank Neville Haack, pp. Leeann Phillips and David Cole for technical assistance Dymock, J.J., Forgie, S.A., 1993. Habitat preferences and carcase throughout, and Lilian Morrison for the statistical colonisation by sheep blowflies in the northern North Island of analysis. Dr Garry Levot provided useful comments on New Zealand. Med. Vet. Entomol. 7, 155–160. an earlier draft of this paper. This work was initially Dymock, J.J., Peters, M.O.E., Herman, T.J.B., Forgie, S.A., 1991. 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