Deer Ked Ectoparasitic Fly Biology Essay

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The deer ked (Lipoptena cervi, L., Diptera, Hippoboscidae) is an ectoparasitic louse fly of the moose (Alces alces) and other cervids. It spread to Finland in the early 1960's from the South-East (Hackman et al., 1983) and at present it is a common parasite in the southern parts of Finland with its northern distribution limit gradually spreading northwards. This means that it will be shortly in contact with another potential host, the semi-domesticated reindeer (Rangifer tarandus tarandus). In the former Soviet Union, the deer ked parasitized practically every moose in Belarus with 1144-5082 keds per moose (Ivanov, 1981) and in the Leningrad region between 200-300 keds per moose with a maximum number of approximately 1000 flies (Popov, 1965). In Poland, this parasite could be found in 93 % of moose, 78 % of red deer (Cervus elaphus), 64 % of roe deer (Capreolus capreolus) (Kadulski, 1996) and 76 % of fallow deer (Dama dama) (Szczurek & Kadulski, 2004). The general public considers the deer ked a pest. It attaches eagerly to human clothing and hair, drops it wings and bites quite often but has not been observed to parasitize humans permanently. However, adverse skin reactions mostly interpreted as allergic are regularly encountered (Rantanen et al., 1982; Reunala et al., 2008).

As a hippoboscid fly, the deer ked is morphologically and physiologically adapted to the ectoparasitic life (Metcalf & Metcalf, 1993). It is dorsoventrally flattened with a hard exoskeleton. It drops its wings immediately upon attachment on the host (Hackman et al., 1983) and has large claws to enhance the attachment and to prevent detachment (Haarløv, 1964). The deer ked is a pool feeder: it cuts the skin of the host and consumes the blood accumulating in the wound. The reproductive strategy of the deer ked is viviparous (Meier et al., 1999). The egg hatches in the reproductive tract and the developing larva is fed by secretions produced by the female. One female can produce 20-32 pupae (Popov, 1965; Ivanov, 1981), slightly more than the related sheep ked (Melophagus ovinus) (Metcalf & Metcalf, 1993). The pupae fall from the fur of the host to the forest floor or snow and during the next autumn the adult flies emerge (Popov, 1965). The deer ked does not fly actively searching for a host but stays close to its hatching site and waits for a suitable host to arrive. Between 14-24 °C the flight distance is ad 50 m, at 7-11 °C up to 15 m and below 7 °C keds become inactive. The deer ked has one generation per year, the emergence of adults starts at the end of July and the flight season ends at the beginning of November (Ivanov, 1981). A deer ked lives for 120-180 days after it has selected a host. The adults die out gradually and from February-March moose remain unparasitized until the next autumn (Popov, 1965).

The aim of this study was to determine the basic patterns and characteristics of deer ked parasitism on the moose in Eastern Finland. The specific aims were to study 1) how the age and sex of the moose affect the parasitism and 2) how the density of deer keds differs between anatomical regions of the moose skin. It can be hypothesized that the deer ked would be present in high numbers on Finnish moose and that the selection of an anatomical region of the host would depend on, e.g., fur characteristics such as hair length.

Materials and methods

Whole moose skins (n = 23) were collected during the legal hunting season between October 7 and November 26, 2006 in Liperi commune, Eastern Finland (62°31'N, 29°08'E). The age, sex and general condition of the moose were determined. The body mass was estimated from the weight of the carcass (Wallin et al., 1996). The thickness of subcutaneous fat reflecting the nutritional state was measured from an incision in the gluteal region after skinning as instructed by the Finnish Game and Fisheries Research Institute (2009a). Immediately after skinning, the skin was divided into six sections (head, anterior back, posterior back, front limbs, hind limbs and abdomen; Fig. 1) based on the anatomical region and the length of the fur (Sokolov & Chernova, 1987). Each section was sealed in a plastic bag and frozen at -20°C. In the laboratory, the hair was cut with scissors and all keds and other arthropod ectoparasites were collected by hand. The area of the skin was determined by placing a metal grid (20 Ã- 20 mm) on a skin section and calculating the number of squares covering the section.

The deer keds were divided into categories as follows: recently attached winged, recently attached wingless, blood-consumed (expanded abdomen containing blood), copulating pairs (always blood-consumed ones) and pupae. Other arthropod parasites were also determined. A random subsample (n = 200 unless the total number/section was less) of all sections was divided by sex. Both sexes were individually weighed and the mean weights of the deer keds of both sexes were calculated. Based on the sex ratio and the mean weights of the male and female keds the total numbers of flies of both sexes on each skin section were estimated.

Comparisons of the total numbers of deer keds and their densities per skin area according to the age, sex and different anatomical regions of the moose were performed with the one-way analysis of variance (ANOVA) and the Duncan's post hoc test with the SPSS-program (v. 15.0, SPSS Inc., Chicago, IL, USA). For nonparametric data, the Kruskal-Wallis ANOVA on ranks followed by the Dunn's post hoc test was performed with the SigmaPlot-program (v. 11.0, Systat Software Inc., San Jose, CA, USA). Correlations were calculated with the Spearman Correlation Coefficient (rs). A p-value < 0.05 was considered statistically significant. The results are presented as the mean ± S.E.

Results

The load of deer keds on the moose was high and varied depending on the sex and maturity of the host. The bulls had on the average 10616 ± 1375 deer keds, the cows 3549 ± 587 keds and the calves 1730 ± 191 keds, all these values being significantly different from each other (Table 1). The maximum numbers of deer keds on the bulls, cows and calves were 17491, 5130 and 2309, respectively (Table 2). The bulls had more copulating deer ked pairs and pupae than the cows and calves. Other ectoparasites were scarce with only few ticks (Acari) present.

The bulls had more keds per skin area than the cows and calves (Table 3). The density of deer keds was the highest on anterior back, where approximately half of all keds were found (Table 4, Fig. 1). This was followed by posterior back with approximately one fourth of all keds. The density on other regions decreased according to the sequence: front limbs > abdomen > head > hind limbs. The numbers of recently attached winged and wingless deer keds and their densities correlated negatively with the date of sampling (rs = -0.712- -0.936, p < 0.01), while the number of copulating pairs on the bulls correlated positively with the sampling date (rs = 0.795, p < 0.05). The thickness of gluteal fat did not correlate with the numbers or densities of deer keds.

The sex ratio of the deer keds was equal (1:1) in all anatomical regions. Weights of recently attached winged and wingless keds did not differ significantly but blood-consumed keds were heavier (Table 5). After deer keds had consumed blood, males were heavier than females. The mean weight of pupae was 9.996 ± 0.391 mg. The weights of the deer keds did not differ according to the age, sex or anatomical region of the moose.

Discussion

The total numbers and densities of deer keds on the moose were extremely high. The examined moose had 1.5-2.1 times more deer keds than reported for the moose in Soviet Belarus (Ivanov, 1981), 9-35 times more than on the moose in the Leningrad region of the former Soviet Union (Popov, 1965) and 115-708 times more than on the red deer in Denmark (Haarløv, 1964). The deer keds were much more numerous than reported previously for other louse fly species on homeothermal animals. The maximum number of sheep keds was 300-400 keds per sheep (Ovis aries) (Legg et al., 1991), while the number of louse flies on birds seems to be smaller as, for example, the maximum number of Crataerina pallida on the European swift (Apus apus) was 31 flies (Hutson, 1981). Some homeothermal animals seem to be able to resist hippoboscid parasitism. After experimental infections of 50-1000 parasites followed by a period of parasite reproduction, sheep seemed to be able to develop partial resistance and the number of sheep keds declined to < 50 keds per animal (Nelson, 1962). In a similar manner, after experimental infections of deer keds on reindeer, only 1-18 of the original 300 keds per reindeer survived (Kynkäänniemi et al., unpublished data). As the moose of the present study were so heavily parasitized, any similar resistance would be unlikely.

There are no reports on other louse fly species on the moose that would be as numerous as the deer keds in the present study, but in North America winter ticks (Dermacentor albipictus), a one-host parasite overwintering on wild cervids (Mooring & Samuel, 1999), were reported to be present at the number of 30000 ticks or more per moose (Samuel & Welch, 1991). This parasite caused weight loss, anaemia and possibly secondary bacterial infections for captive moose (Glines & Samuel, 1989). Parasitism of winter ticks caused nuisance and moose tried to remove ticks by grooming, which increased hair loss (Mooring & Samuel, 1999). Winter ticks preferred shoulders, neck and withers similar to the deer keds in our study and hair loss began and was the most severe on these regions. The grooming rate and hair loss were connected to the developmental stage of ticks; adult ticks irritated moose more than nymphal stages (McLaughlin & Addison, 1986). Hair loss remained at a low level until February, in March it increased sharply and peaked in April and May (Mooring & Samuel, 1999). In our study, only one moose had minor hair loss (approximately 5 dm2), which suggests that deer ked parasitism at the observed level would not cause alopecia for moose, but more studies in winter and spring will be needed to confirm this. Furthermore, the load of deer keds was not inversely associated with the estimate of body adiposity unlike observed previously in winter tick-infested moose suffering from hair loss (McLaughlin & Addison, 1986).

The mean density of cattle biting lice (Bovicola bovis) on steers (Bos taurus) was 26.5 lice per skin dm2 (data calculated from Watson et al., 1997), which was less than the mean deer ked density on the bulls in the present study. The highest B. bovis densities on steers were on poll and shoulder regions (88.6 and 79.5 per skin dm2), which were higher than the mean deer ked densities on anterior back of the moose in the present study. Arthropod ectoparasites could be found in 44 % of domestic dogs (Canis familiaris) (Aldemir, 2007) and 82 % of domestic cats (Felis catus) were parasitized by Ctenocephalides felis with a mean of 16 parasites per cat when using the random sampling method of minor areas (Hsu et al., 2002). Over 45 % of all fleas were located on head and neck regions, the next preferred region was dorsal with over 27 % of the fleas. The sheep ked preferred rib and shoulder regions (Legg et al., 1991) and the sheep with an open, long and fairly greasy fleece were considered ideal hosts for the sheep ked (Evans, 1950). The deer ked displays negative geotaxis and phototaxis (Ivanov, 1981), which may explain why most of the keds were attached to the withers of the moose. The fur is the longest in the withers, up to 200 mm (Sokolov & Chernova, 1987), which could provide the best shelter for keds.

According to Kadulski (1974), the degree of deer ked parasitism correlated positively to the body size of the host. In the present study, the adult moose had more keds than the calves, which fits the hypothesis, but the bulls had more keds than the cows, despite of no significant differences in the skin area and of the slightly lower body mass. Based on the natural history of the deer ked, the moose with large home ranges and high levels of activity could have the highest risk to become parasitized. In Finland, 64 % of all bulls move more than 15 km between seasonal home ranges, while only 30 % of cows travel as far (Heikkinen, 2000). The moose travel several times between summer and winter home ranges before settling in their winter habitats. Therefore the bulls could have de facto larger home ranges in autumn, which may partly explain why they had higher numbers of deer keds on their skins. In the present study, the cows had higher numbers of keds than the calves, but the densities of deer keds between these two groups were equal. Ivanov (1975) noticed that if two potential hosts of different size were in the vicinity, the deer keds chose the bigger one. Based on this, calves that still follow their dams may attract less keds.

The negative correlation between the total numbers and densities of recently attached deer keds and the sampling date were logical when reckoned with the flight season of the deer ked. The numbers of recently attached winged and wingless keds were minor on the moose skins, as almost all keds had consumed blood by the time of the sampling. Recently attached wingless deer keds were slightly heavier than recently attached winged keds indicating that wingless keds had already consumed blood, although they did not yet show the distended abdomen characteristic to the majority of keds. In the Leningrad region of the former Soviet Union the mean weight of the newly hatched deer keds was 8-9 mg, and a weight loss of 3.0-3.5 mg was considered fatal (Popov, 1965). In the present study, recently attached deer keds were over 50 % lighter than deer keds in the Leningrad region. This indicates that there could be significant variation in the weight of deer keds between different geographical regions. This has to be confirmed in the future as it is not impossible that some vaporization could have occurred during the storage of the keds.

Based on our results, we can preliminarily estimate the population size of deer keds in Finland. The mean number of deer keds was 5400 keds per moose. Based on the equal sex ratio (present study) and the reproductive outcome of the deer ked (Popov, 1965; Ivanov, 1981), these 5400 deer keds could hypothetically produce 54000-86400 pupae annually. According to the Finnish Game and Fisheries Research Institute (2009b), the size of the moose population in Finland was 79000-93000 individuals after the hunting season in 2006. These moose could host 400-500 million deer keds that could produce 4-8 billion pupae. Ivanov (1981) estimated that in 1972 the size of the deer ked population in Belarus was 36 million keds, much smaller than the estimated population size in Finland. The number of deer keds correlated positively with the population size of the moose, while the numbers of roe deer and red deer did not affect the size of the deer ked population (Ivanov, 1981). In Eastern Finland the sizes of the populations of other cervids are notably smaller than that of the moose population (Juha Kuittinen, personal communication). This together with results of Ivanov (1981) suggest that the moose could be the principal host of the deer ked. Based on this, reducing the number of moose may be the most practical way to control the size of the deer ked population.

Conclusions

1) The moose were heavily parasitized by the deer keds. The calves had less keds than the adults possibly due to the tendency of deer keds to choose a host of a larger body size, and the bulls had more keds than the cows, which could be caused by their more active travel between seasonal home ranges. 2) The density of deer keds varied between the different anatomical regions being the highest on anterior back, where half of all keds were located. This could be explained e.g. by the long hair on the region of the withers or by the negative geotaxis and phototaxis displayed by deer keds. The level of parasitism was so high that the effects of the deer ked on the health of cervids should be determined.

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