Failure of two consecutive annual treatments with ivermectin to eradicate the reindeer parasites ( Hypoderma tarandi , Cephenemyia trompe and Linguatula arctica ) from an island in northern Norway

The highly efficient endectocide ivermectin is used to reduce the burden of parasites in many semidomestic reindeer herds in northern Fennoscandia. In the autumn of 1995 and 1996 all reindeer on the island of Silda (42 km2) were treated with ivermectin in an attempt to eradicate the warble fly (Hypoderma (=Oedemagena) tarandi (L.)), the nose bot fly (Cephenemyia trompe (Modeer)) (Diptera: Oestridae) and the sinus worm (Linguatula arctica Riley, Haugerud and Nilssen) (Pentastomida: Linguatulidae). Silda is situated 2-3 km off the mainland of Finnmark, northern Norway, and supports about 475 reindeer in summer. A year after the first treatment, the mean abundance of H. tarandi was reduced from 3.5 to 0.6, but a year after the second treatment the mean abundance unexpectedly had increased to 4.5. After one year without treatment, the mean abundance and prevalence of the three target parasites were at the same level, or higher, than pre-treatment levels. The main hypothesis for the failure to eliminate the parasites is that gravid H. tarandi and C. trompe females originating from untreated reindeer in adjacent mainland areas dispersed to the island during the warm summer of 1997 (possibly also in 1998). As these oestrids are strong flyers, it may not be too difficult for them to cross >2-3 km of oceanic waters. There are no good explanations for the failure to eradicate L. arctica, but the results indicate that there may be elements in its life cycle that are unknown. The conclusion of the study is that it may be difficult or impossible to eradicate these parasites permanently, even locally such as on islands unless adjacent areas on the mainland are also cleared.

In the reindeer industry, ivermectin is primarily used to suppress high larval burdens of H. tarandi and C. trompe.Reindeer are treated once a year, in late autumn or early winter, and as a rule, mostly calves are treated (Haugerud et al., 1993, Nilssen et al., 1999).
Oestrids of cattle and reindeer are extremely sus¬ ceptible to treatment with ivermectin, and there is approximately a 1000-fold overkill when the rec¬ ommended dose of 0.2 mg/kg is used in cattle (Baron & Colwell, 1991).Because of this high effi¬ ciency, and the eradication of cattle grubs in other countries, the objective of this study was to deter¬ mine if herd treatment with ivermectin would result in eradication of H. tarandi and C. trompe from an island in northern Norway.In addition, the pentastomid L. arctica was included.
It is expensive and logistically difficult to treat all reindeer in a large area (e.g. the county of Finnmark in Norway, or similar areas).Treating all reindeer in single herds is possible, but there may be risks of "invasions" of flies originating from neighbouring, untreated or partly treated herds.Reindeer oestrid flies are good fliers and experi¬ mental studies with oestrid flies have shown a flight capacity of several hundreds of km (Nilssen & Anderson, 1995); the longest recorded distances flown in the field (released and recaptured flies) were 90 and 45 km for H. tarandi and C. trompe, respectively (Gomoyunova, 1976).About 25 years ago, (Kummeneje, 1976;1979) tried to eradicate reindeer oestrids on islands in northern Norway with Warbex (a systemic organophosphorous insecticide), an antiparasitic drug less efficient than ivermectin.He succeeded in sup¬ pressing the H. tarandi populations by 94-99% on a few islands, but the populations increased to "normal" just two years post treatment.He con¬ cluded that 100% elimination was necessary.Complete eradication was probably impossible with Warbex due to its poor efficiency, but it was thought that, with proper administration, eradica-tion might be possible with any of the highly effi¬ cient new endectocides like ivermectin.Since the parasites included in this study are host specific and confined within the host at known times, they should theoretically be easy to eradicate in an erad¬ ication programme.

Study area
The island of Silda was chosen as the target location for this eradication experiment.This island, situat¬ ed 2-3 km from the nearest adjacent mainland, also was one of the islands used in the previous eradica¬ tion study 25 years ago (Kummeneje, 1979).Silda is a small island (70°19'N; 21°45'E) near the coast of western Finnmark, northern Norway.It is 15 km long, and has an area of 42 km 2 and it is part of reindeer pasture district 29 of West-Finnmark.Until some years after World War II, the island supported several small farms and a small fishing village, but the island no longer supports any per¬ manent human settlements.The island is dominat¬ ed by steep mountains, which reach an altitude of 628 m a.s.l., and most areas are almost inaccessible (Alm & Gamst, 1997).
The island is used as summer pasture for approx.475 reindeer.These reindeer spend winter inland close to the border of Finland.In April the herd migrates northward towards the coast of the main¬ land, from where the reindeer are transported to Silda by ship in early May.Oestrid larvae drop from reindeer from late April to late June (Nilssen & Haugerud, 1994); consequently, the reindeer trans¬ fer the majority of their oestrid parasites to the summer grazing pastures on the island.Later, when the adult oestrid flies have emerged from the puparia and mated, they may easily come in close contact with their host because the herd remains on the island until September-October.Reindeer herders have at times observed intense harassment by the oestrids, especially during warm summers (Oddvar Sara, pers. comm.).

Treatment and monitoring
The experiment started in late November 1995, after the entire herd of 473 reindeer from Silda had been moved towards the winter grazing area near Kautokeino in the inner (continental) area of Finn¬ mark (a distance of about 180 km).The initial pretreatment levels of parasites were determined from samples obtained from 30 slaughtered reindeer.Sampling for H. tarandi was carried out by count¬ ing second instar larvae under the skin on raw hides of all the slaughtered animals (as described by Folstad et al., (1989)).The heads of all slaughtered reindeer were frozen and transferred to the laboratory where L. arctica was sampled by examining the sinuses (see Haugerud, 1988), and first instars C. trompe were sampled with a rinsing-sieving technique described by Nilssen & Haugerud (1995).
Shortly after the seasonal slaughtering, all animals in the remainder of the herd were injected subcutaneously with a standard dose, 0.2 mg/kg body weight, implying a solution of 1 ml for small calves, 2 ml for normal adults, and 3 ml for large adults of injectable ivermectin (Ivomec veterinary injection 10 mg/ml; Merck, Sharp & Dohme B. V., Haarlem, Holland).A veterinarian ensured that all animals in the herd were treated.A green paint was applied to mark each treated animal.
After its seasonal northward migration in spring 1996, the herd was shipped to Silda, where it spent the summer.On 25 November 1996 (one year post treatment), all slaughtered animals (» = 52) were sampled for H. tarandi (C.trompe and L. arctica were not sampled this year).The remainder of the herd (those not slaughtered) was treated with ivermectin as described above.Migrating reindeer again were shipped to Silda in the spring of 1997, and on 19 December 1997, the same sampling procedure used in 1996 was repeated.Again, only H. tarandi was sampled (n =65, i.e. all slaughtered animals).This sampling provided the infestation levels one year after two consecutive treatments.Reindeer were not treated with ivermectin in December 1997.However, animals that spent the summer of 1998 on Silda were again sampled on 1 February 1999 when H. tarandi, C. trompe and L. arctica were sampled in the same way as described above, after which the experiment was terminated.Parasitological terminology is in accordance with Bush (1997).

Summer temperatures during the infestation periods
Daily air temperature data (measurements at 0700, 1300 and 1900h) for the infestation period (July and August) for 1996, 1997 and 1998 were obtained from The Weather Bureau of North Norway for two weather stations, Loppa and Tromsø.The island of Loppa is situated about 12 km from the centre of Silda, but has a position more isolated in the ocean so that the climate is more oceanic with lower maximum temperatures than Silda and its adjacent mainland.Because there are no other meteorological stations close to Silda, the data from Loppa was combined with a more distant station.Although it is situated ca 150 km southwest of Silda, Tromsø was chosen because this station has an oceanic climatic influence probably more comparable with that of Silda than the climate of Loppa.Each pairs of contemporary temperatures from these two stations were averaged and used in the analyses.

Results
After the first treatment both mean abundance and prevalence of H. tarandi were considerably reduced in 1996, but this parasite was not eradicated completely (Fig. 1).C. trompe was not sampled in 1996, partly because of practical reasons, but also because the abundance of H. tarandi indicated that larvae of C. trompe would be scarce.Normally, the mean abundance of C. trompe is much lower than that of H. tarandi.The pre-treatment mean abundance of C. trompe was only 22.6% of that of H. tarandi (Table 1), which is nearly identical to previous results in 327 reindeer in northern Norway in 1988 and 1989 when the corresponding figure was For details, see Table 1.18.7% (Nilssen et al., 1998).Based on these results, the mean abundance of C. trompe would have been: 0.58 x 18.7% = 0.11 in 1996.Among the 52 reindeer sampled therefore, we would expect only 52 x 0.11 = 6 C. trompe larvae.
Sampling for the three parasite species at two years after the last treatment revealed that all were present (none had been eradicated).For all three species, the mean abundance was higher than before the first treatment in 1995.
When the months of July and August are com¬ pared for temperatures at 1300h, the summers of 1996, 1997 and 1998 (the infestation years for the three last samplings) were different (Fig. 2).In 1996 August was the warmest summer month.In 1997 and 1998, however, July was the warmest.

Discussion
Although ivermectin is a highly efficient antiparasitic drug, two consecutive annual treatments of the entire reindeer herd on the island of Silda did not eradicate any of the targeted parasite species.After the first treatment, the population of H. tarandi was considerably reduced, but not com¬ pletely eradicated.After the second treatment, a further reduction in the H. tarandi population was expected but on the contrary, the mean abundance was higher than before the treatment started.The further increase observed 26 months after the sec¬ ond treatment (the sampling in 1999, which reflects the infestation in 1998), may be attributa¬ ble to climatic factors, as it has been shown that larval burdens of reindeer oestrids vary greatly between years (Nilssen & Haugerud, 1995;Nilssen et al., 1998).Both 1997 and 1998 had favourable temperatures in July when the main infestation occurs.

H. tarandi adult
The most interesting result, and the most diffi¬ cult to explain, is that H. tarandi increased in mean abundance and prevalence from 1996 to 1997.We expected a further decrease, but observed a 7.8-fold increase in mean abundance.We propose three hypotheses for this unexpected result.

The flight immigration hypothesis
The two reindeer oestrids have the capacity of flying long distances (Gomoyunova, 1976;Nilssen & Anderson, 1995), which is considered an advanta¬ geous attribute for species associated with migrato¬ ry hosts (Gomoyunova, 1976;Howard & Conant, 1983, Nilssen & Anderson, 1995).In the case of reindeer oestrids, larvae are often dropped far from the summer grazing land where seasonal infestation occurs.Even during the infestation period the rein¬ deer often move long distances to graze or to avoid oestrid attacks.In the present study, the distance per se is not the problem be¬ cause Silda is only separat¬ ed by 2-3 km from the nearest mainland (Fig. 3).Although Russian resear¬ chers have suggested that reindeer oestrids are un¬ willing to fly over open waters (even a river 500 m wide is thought to be a barrier (Saveljev, 1971)), females of H. tarandi have been observed flying over The flight activity of both reindeer oestrids is dependent on temperature, light intensity and wind (Anderson & Nilssen, 1996b, and references therein).Their lower tem¬ perature threshold for flight is 8-10 °C (if expo¬ sed to direct sunshine), but under most environmental conditions they become active at temperatures exceeding 12-15 °C, and intense harassment of reindeer by the flies is only observed with temperatures >18-20 °C (Anderson & Nilssen, 1996b).In July of 1997 and 1998 tem¬ peratures were frequently > 18 °C.The majority of adults emerge from the puparia in the beginning of July (Nilssen, 1997a), and high temperatures for many days shortly after eclosion, as in 1997 and 1998, are essential conditions to create a mass occurrence of newly emerged flies.Temperature data shows both 1997 and 1998 were typical years when there could be a mass concentration of host¬ seeking oestrids in the period 12 -23 July, and this could account for the dispersal of many flies to off shore islands like Silda.Compared to 1997 and 1998, the late, cool summer of 1996 probably resulted in only small numbers (if any) of H. tarandi and C. trompe dispersing to Silda.
As mated H. tarandi females are known to fly for much longer durations and distances than unmated females (Nilssen & Anderson, 1995), the flight immigration hypothesis implies primarily that such individuals flew from mainland areas to Silda in July 1997.The mainland areas adjacent to Silda are summer grazing areas for untreated reindeer.From the increase in the larval burden of H. tarandi found in 1997, it is believed that from 10 to 100 individuals may have dispersed to Silda.
Flight immigration also may have occurred in 1998 because, as mentioned, the July weather was similar to that in 1997.This second immigration, however, is not required to explain the high larval burden in 1998 because the population in the Silda herd alone in 1997 probably was high enough to give rise to the population size in 1998.

The treatment failure hypothesis
If it is postulated that the reindeer, not slaughtered in December 1996, had the same mean abundance (0.58) and prevalence (13.46%) as the sampled (slaughtered) animals, we can calculate that this remaining herd of 420 reindeer altogether har¬ boured 0.58 x 420 = 244 H. tarandi larvae, and that 420 x 13.46% =57 reindeer were infected.If untreated, 244 would be the maximum estimated number of larvae that could be brought back to Silda, but all these reindeer were treated.The recommended dose of ivermectin used (0.2mg/kg) has a 1000-fold overkill (Baron & Colwell, 1991), so if some reindeer for some reason did not get the full dose, probably all larvae would have been killed.The other possibility is that some reindeer "escaped" treatment.If it is assumed that 12 rein¬ deer (4.9%) were untreated, we would have 0.58 x 12= 7 H. tarandi larvae that could be brought to Silda the following spring (1997).However, it is highly unlikely that this quantity of larvae could give rise to the increased larval burden (mean abun¬ dance 4.5 and prevalence 58%) observed by the end of 1997.If it is postulated a mortality of 20% in the pupal stage occurred it would result in 5-6 adults, and as the sex ratio is 1:1 (Nilssen, 1997a), there would be at maximum three males and three females.If all three females were successfully mated, each with a potential fecundity of 600 eggs (Nilssen, 1997b), there would be a potential of 1800 eggs in total that -if transmitted -could hatch to larvae and infect reindeer.With a mortal¬ ity of 20% during the first larval instar, there would be 1800 x 80% =1440 larvae in the whole herd in November 1997.In 1997 the sampling revealed a mean abundance of 4.5 larvae, or an esti¬ mated number of 470 x 4.5 = 2115 larvae in the whole herd.
Although there are many uncertainties in these calculations, the difference between 1440 and 2115 is such than that there is a possibility that the hypothesised H. tarandi population in 1996, despite treatment, could give rise to the population 120 observed in 1997.However, the figure of 1440 is probably far too high, especially as the realised fecundity is much lower than the potential of 600 eggs per female.As observed earlier, most females do not succeed in depositing all their eggs (Anderson & Nilssen, 1996a).Additionally, it is believed that the proportion of reindeer successful¬ ly treated exceeded 95%, the percentage used in the above calculations.
On the other hand, because total eradication was not achieved after the first treatment, the possibil¬ ity that a few reindeer may not have been treated with ivermectin cannot be ruled out.

The guest reindeer hypothesis
This hypothesis acknowledges that a few untreated reindeer from other herds could have intermingled with the Silda herd during its northward spring migration.The reindeer owner was fully aware of that such an intermingling of reindeer from other herds would ruin the experiment, and consequent¬ ly, did everything to prevent this.After the exper¬ iment, the owner asserted that no "foreign" rein¬ deer were shipped over to the island during the study years.Therefore, our opinion is that the rea¬ soning for this hypothesis is weak.
Due to missing samples we know less about the effect of ivermectin treatment on C. trompe and L. arctica.We know, however, that neither of them was eradicated after completion of the experiment.C. trompe might have been eradicated both in 1996 and 1997, but as it occurred with fairly high num¬ ber in 1998, we hypothesise that, as for H. tarandi, immigration occurred in 1996 or 1997, or in both years.
The fact that L. arctica also was not eradicated is more difficult to explain.The only published test of the vulnerability of L. arctica to ivermectin, is a field experiment that showed nearly 100% efficien¬ cy (Haugerud et al., 1993), but little is known about the dose response.In the present study, as well as in the previous field experiment (Haugerud et al. , 1993), doses adjusted for oestrids were used.If ivermectin, as used against oestrids, is not 100% effective this would explain the failure to eradicate the species.
The life cycle of L. arctica is only partially known (Riley et al., 1987), but it is thought that the species survives the winter within the host, and that the eggs, which are deposited in summer, do not survive the winter.Fresh eggs do not withstand frost (R. E. Haugerud, unpubl.data), but older eggs (i.e.eggs not transmitted to reindeer) may have increased cold hardiness.If so, older eggs Rangifer, 22 (2), 2002 might have survived one or two winters before infecting the host.Consequently, it would be nec¬ essary to treat more than two years in succession, as was done the present experiment.
Whatever the explanation for the failure to erad¬ icate the three parasite species, the experiment shows, as with similar experiments, that parasites are often difficult to eradicate under natural condi¬ tions.Several previous studies have shown that even under intense control pressure, oestrid popu¬ lations have an unexpected ability to rebound to pre-control levels (Rich, 1965;Breyev, 1973;Kummeneje, 1979;Scholl et al., 1986), most prob¬ ably because of their great dispersal potential, their high efficiency to transmit their progeny to the host, and, not the least, their high fecundity and the decreased immune response in hosts deprived of antigenic stimulation through contact with the parasite.
Previous eradication trials, and the present study, show that a nearly 100% elimination is nec¬ essary if the aim is to eradicate the parasite.A per¬ manent eradication will, however, not be achieved if there are possibilities for immigration.If the flight immigration hypothesis for the present study is correct, which is virtually certain, better results would be obtained if the experiments were carried out on islands that are more distant from the main¬ land.

Fig. 1 .
Fig. 1.Graphical illustration of the eradication experiment.Effect on parasite burden following ivermectin treatment of all reindeer on the island of Silda.For details, see Table1.

Fig. 3 .
Fig. 3. Map showing the islands of Silda and Loppa (where one of the meteorological stations was located) and adjacent mainland areas.The figure illustrates the flight immigration hypothesis: H. tarandi females originating from lar¬ vae dropped from untreated reindeer on the mainland were able to fly over oceanic water to infect treated reindeer on Silda in July 1997 (also possibly in July 1998).Female C. trompe also likely dispersed to Silda in 1997 or 1998, or in both years.

Table 1 .
Mean abundance and prevalence of oestrids and L. arctica before and after treatment of all reindeer on the island of Silda.The sample size (n) corresponds to all slaughtered reindeer.C. trompe and L. arctica were not sampled in 1996 and 1997.