ORIGINAL RESEARCH

 

Helminth parasites of impalas, Aepyceros melampus, in eastern southern Africa, collected during 1973 to 2007

 

 

IG Horak^I; K Junker^II; LEO Braack^{III, IV}; GJ Gallivan^V

^IDepartment of Veterinary Tropical Diseases, Faculty ofVeterinary Science, University of Pretoria, South Africa
^IINational Collection of Animal Helminths, Epidemiology, Parasites and Vectors Programme, ARC-Onderstepoort Veterinary Institute, South Africa
^IIIMalaria Consortium, Faculty of Tropical Medicine, Mahidol University, Thailand
^IVInstitute for Sustainable Malaria Control, Faculty of Health Sciences, University of Pretoria, South Africa
^V43 Leeming Drive, Canada

Correspondence

 

 

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ABSTRACT

This paper summarises published and unpublished data on helminths collected systematically from 424 impalas at 11 localities in eastern southern Africa, from St. Lucia in KwaZulu-Natal (KZN) to the Tuli Block in north-eastern Botswana. It includes data on collections in the Kruger National Park (KNP) in the drought of 1982, and in 1992/93 following the 1991/92 drought. Thirty-three species of nematodes, plus six taxa identified only to the generic level, three taxa of trematodes, and three species of cestodes were collected. Helminth species richness was highest in the southern KNP and lowest in the Tuli Block. The prevalence and intensity of infection of several helminths also declined from KZN and the southern KNP to the drier areas in the north and west. With the exception of St. Lucia and Nylsvley, > 80% of the helminths collected at each locality were collected in the southern KNP. St. Lucia was the most dissimilar locality; of the 20 helminths collected, five were unique. Ten of 33 species of nematodes, the paramphistomines (Trematoda) and the cestode Stilesia hepatica were collected at seven or more localities. Six of the most common nematodes, Cooperia hungi, Cooperioides hamiltoni, Impalaia tuberculata, Longistrongylus sabie, Strongyloides papillosus and Trichostrongylus deflexus are primarily parasites of impalas in the southern KNP, whereas many of the helminths collected at only one or two localities are parasites of other hosts. Nematode burdens were increased in the drought affected impalas in 1982, but helminth burdens decreased in 1992/93 following a dry cycle.

Keywords: zooparasitic Nematoda, Cestoda, Trematoda, prevalence, distribution, drought

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Introduction

Impalas, Aepyceros melampus, are medium-sized, lightly built antelope widespread in the eastern parts of Africa (Skinner & Chimimba 2005). In South Africa, impalas occur mainly in the provinces of Limpopo, Mpumalanga, North West, Gauteng, and the north-eastern KwaZulu-Natal (KZN).

According to Round (1968), two trematode and two cestode species, a larval cestode, 16 nematode species and a nematode genus occurred in impalas in South Africa. Most of these records were for parasites collected incidentally or during culling operations (Meeser 1952; Young & Wagener 1968). Since then, there have been a number of reports (Horak 1978; Anderson 1983; Boomker, Horak et al. 1989b; van Wyk & Boomker 2011) based on the systematic collection of the helminths of impalas that provide quantitative estimates of the prevalence and intensity of infection at various localities in South Africa. Negovetich et al. (2006) examined the infracommunities and component communities of nematodes infecting the impalas at three localities, Skukuza, Biyamiti and Crocodile Bridge, in the southern Kruger National Park (KNP) from 1980 to 1982, but did not discriminate between localities, nor consider the potential effects of the drought that occurred in 1982. Horak et al. (2023) re-examined the data from Skukuza and Biyamiti, and compared the differences in prevalence and intensity of infection in helminths between the two localities by age, sex and month.

In addition to the collections in the southern KNP in 1980 and 1982, IGH was able to collect helminths from impalas at Pafuri in the north of the KNP in 1977 and 1980, and Prof J Boomker from animals on the research farm 'Delftzyl' in Limpopo Province. We (IGH, LEOB) also collected helminths from impalas at Skukuza, Crocodile Bridge and Pafuri in 1992/93, at the end of, and after, the 1991/1992 drought. An unknown collector, whom we have been unable to trace, also provided collections of helminths from impalas in the Tuli Block (North Tuli and South Tuli) region of north-eastern Botswana. The collections in 1977 and 1980 at Pafuri, 1992/1993 in the KNP, at Delftzyl, and in the Tuli Block are unpublished, and as noted above, Negovetich et al. (2006) combined localities and years in their analyses, thus the collections from Crocodile Bridge in 1980 and in the southern KNP during the 1982 drought are also unpublished.

The unpublished collections, plus the previously published reports of Horak (1978), Anderson (1983), Boomker et al. (1989b), van Wyk and Boomker (2011) and Horak et al. (2023) provide information on the helminths of impalas throughout South Africa, from north-eastern KZN to the northern tip of the KNP and into north-eastern Botswana. The collections encompass a range of habitats, with annual rainfall ranging from approximately 900 mm in KZN to 300-400 mm in the north of the KNP and the Tuli Block. This paper compares the differences in helminth species prevalence and intensity of infection among the various localities, and assesses the impact of the droughts of 1982 and 1991/92 in the KNP.

 

Materials and methods

Study areas

The localities (Figure 1), the vegetation type, and the number of and frequency with which the impalas were examined at each locality are presented in Table I. All of the localities are within the summer rainfall region of southern Africa. Rainfall is variable with wet cycles and dry cycles, and is subject to periodic droughts (Tyson 1978). The annual rainfall at Skukuza in the KNP over the period of all collections, including those of Anderson (1983) and van Wyk and Boomker (2011), is shown in Figure 2. The period contained two wet cycles, from 1972 to 1981, and 1993 to 2002, and two dry cycles, from 1982 to 1991/1992, and from 2003.

 

 

 

 

Parasite collection

The methodology for parasite collections in the published papers is described by the authors (Horak 1978; Anderson 1983; Boomker et al. 1989b; van Wyk & Boomker 2011; Horak et al. 2023). The methodology used for the unpublished collections at Pafuri, at Crocodile Bridge in 1980, in the 1982 and 1992/93 droughts, and at Defltzyl was described by Horak et al. (2023). We are unable to determine the exact methods by which the impala were processed for helminth recovery in the Tuli Block, but the identification of helminths and counting procedures were as described by Horak et al. (2023).

Effect of drought

The collections included two drought periods, the first in 1982, and the second in 1991/1992. The 1982 drought followed a year of low rainfall in 1981/1982, with below average rainfall in the winter and spring of 1982. This was preceded by a period of above average rainfall from 1971 to 1981 (Fig. 2). Drought-affected impalas were collected from October to December 1982 at Skukuza, Biyamiti and Crocodile Bridge in the southern KNP (Table I). Impalas that did not appear to be affected were also collected at Skukuza. The collections in 1992/1993 followed a period of below average rainfall from 1982 to 1992, with the lowest rainfall in 1991/1992 and slightly above average rainfall in 1992/1993. Impalas were collected at Skukuza, Crocodile Bridge and Pafuri (Table I) from February 1992, at the end of the dry year, until May 1993. Thus, the 1992/1993 collections not only included the end of the drought year, but also the recovery period in a year of above average rainfall.

Statistical methods

Factors of interest in the analysis of the data were the differences among localities and the effect of drought. However, it was not possible to compare directly among localities because only aggregate data was available for the helminth burdens in the Nyala Game Ranch (NGR) (Anderson 1983) and St. Lucia (Boomker et al. 1989b) in KZN. Individual animal data were available for the other localities, but the collections were independent and factors that potentially affect helminth burdens, such as age, month and sex (Horak et al. 2023), were not balanced across localities. Therefore, the data were analysed using exploratory data analysis techniques to describe patterns and trends, with extensive use of graphical analysis to assess differences.

Differences in prevalence were analysed using contingency tables with a χ² and logistic regression. For differences in the intensity of infection, the parasite count data were logarithmically transformed to reduce the inequality of variance created by overdispersion (Petney et al. 1990). The data were then analysed using analysis of variance. When factors were significant, a t-test was used to test between two groups and a Student-Newman-Keuls multiple range test was used to compare among multiple groups. When factors such as age, sex and month potentially affected the interpretation, secondary analyses were conducted with restricted data sets to balance those factors when possible. For example, for the 1982 drought, drought-affected and non-drought-affected impalas were compared to age-sex matched controls from November and December 1980 at Skukuza. For the 1992/93 drought, only yearling males were collected at Skukuza; these were compared to yearling males collected at Skukuza in 1980. However, at Crocodile Bridge, yearling and adult males were collected in February 1992 and adult males and females were collected in May 1993. These were compared to adult males, the only age-sex class collected, in 1980.

Impalas less than two years old were aged to month and were classed as lambs (0-11 months), yearlings (12-23 months) or adults (older than 24 months) in the analyses.

 

Results

The unpublished and published collections included 424 impalas. Thirty-three species of nematodes plus six taxa identified only to the generic level, three taxa of trematodes, and three species of cestodes were collected.

The localities at which the helminths were collected are shown in Table II, although not all helminths were collected at a given locality each time when there were collections in multiple years at that locality. Table III lists the prevalence and intensity of infection of the helminths, excluding the drought years of 1982 and 1992/93. Helminth species richness and similarity were highest in the southern KNP, with 23 species at Skukuza and Crocodile Bridge, and 24 species at Biyamiti (Table IV). Species richness was lowest in North Tuli (eight species), South Tuli (11 species) and the northern Limpopo Province (nLP; 12 species). At most localities, > 80% of the species were also collected at Skukuza and Biyamiti. The greatest dissimilarities in species were at St. Lucia and Nylsvley where only 45% and 62.5% of the species that were collected at Skukuza and Biyamiti were present, patterns that were consistent in comparison to the other localities. Five of the 20 helminths at St. Lucia, Cooperia yoshidai, Dictyocaulus viviparus, Trichostrongylus angistris, Trichostrongylus instabilis and the genus Ostertagia, were only collected there, as were three of the 16 species at Nylsvley, Gongylonema pulchrum, Haemonchus placei and Fasciola gigantica.

All of the species collected at North Tuli were collected at Biyamiti, as were nine of the 11 species collected at South Tuli and 11 of 12 in the nLP. However, < 55% of the species collected at North Tuli and South Tuli were collected at the Nyala Game Ranch (NGR), Nylsvley and St. Lucia.

Nematodes

All of the impalas (n = 424) were infected with adult nematodes except one new-born lamb at Skukuza and three females of unknown age at South Tuli.

Ten of the 33 species of nematodes identified may be considered widespread as they were collected at seven or more localities. Cooperioides hamiltoni and Impalaia tuberculata were collected at all eleven localities, Cooperia hungi, Cooperioides hepaticae and Oesophagostomum columbianum were collected at ten, and Longistrongylus sabie, Strongyloides papillosus and Trichostrongylus deflexus were collected at eight, while Cooperia fuelleborni and Trichostrongylus falculatus were collected at seven.

Sixteen species had more restricted distributions. Haemonchus bedfordi and Haemonchus contortus were collected at three localities, Agriostomum gorgonis, Cooperia neitzi, Haemonchus vegliai, Longistrongylus schrenki and Trichostrongylus axei were collected at two localities, and Bunostomum trigonocephalum, C. yoshidai, D. viviparus, G. pulchrum, H. placei, Longistrongylus namaquensis, Nematodirus spathiger, T. angistris and T. instabilis were only collected at one locality.

Nematode burdens

With the exception of the lungworms, P. calcaratus and D. viviparus, all of the nematodes were in the gastrointestinal tract. The prevalence of P. calcaratus was > 83% in the southern KNP based on the presence of eggs, and 98% in the NGR based on the presence of lesions in the lungs. Dictyocaulus viviparus was collected from one impala (20%) at St. Lucia.

The arithmetic mean intensity of infection of adult gastrointestinal nematodes was 4-5 times higher in the NGR than at Skukuza and Biyamiti, while the arithmetic mean at St. Lucia was similar to that at Pafuri (Table III). The prevalence of 11 of the 14 species of gastrointestinal nematodes at the NGR was > 90%, and the intensity of infection of eight species was > 2 times the intensity at Skukuza and Biyamiti. The log-transformed mean intensity of infection did not differ significantly between Skukuza, Biyamiti, Crocodile Bridge, Nylsvley, South Tuli and Pafuri (p > 0.05), but was lower at North Tuli, Delftzyl and the nLP (p = 0.001).

The 10 most widespread species of nematodes accounted for > 90% of the nematodes in the KNP, Tuli Block and Delftzyl, 80.2% in the nLP, 72.8% at Nylsvley, 43.0% in the NGR, and 27.4% at St. Lucia. Trichostrongylus deflexus, C. hungi and C. hamiltoni accounted for > 66% of the gastrointestinal nematodes in the southern KNP and > 95% in the Tuli Block. They were also common at Pafuri, and C. hungi and C. hamiltoni were common at Delftzyl and Nylsvley, while C. hungi was the most numerous species in the nLP. The prevalence of T. deflexus was > 80% in the KNP and Tuli Block, but only 40% in the nLP and 5% at Delftzyl. The intensity of infection in the nLP and at Delftzyl was < 10% of that in the KNP and Tuli Block. Trichostrongylus deflexus was not collected in the NGR, St. Lucia or Nylsvley. Trichostrongylus colubriformis was the most numerous adult nematode at the NGR, accounting for 53.8% of the adult gastrointestinal nematodes, and the second most numerous at Nylsvley (23.7%), but was only collected from three impalas (17.6%) at Crocodile Bridge in 1992/93, three (15.0%) at Delftzyl and two (20%) in the nLP. The arithmetic mean intensity of infection was 11 033 in the NGR, 1 113 at Nylsvley, 88 in the nLP, and < 10 at Delftzyl and Crocodile Bridge.

The prevalence of C. hungi was > 80% in the KNP, Nylsvley and the nLP, and 78.0% in the Tuli block, but was only 65% at Delftzyl and 40% in St. Lucia; C. hungi was not collected at the NGR. The intensity of infection was highest in the southern KNP and South Tuli, and lowest in the nLP and Delftzyl (p < 0.001). The arithmetic mean was lowest at St. Lucia. The prevalence of C. hamiltoni was > 80% in the KNP, South Tuli, Nylsvley, the NGR and St. Lucia, 65% at Delfzyl, 44.4% at North Tuli and 20% in the nLP. The intensity of infection did not differ among localities in the KNP, South Tuli and Nylsvley, but was significantly lower in the nLP and at North Tuli and Delftzyl (p < 0.001). The arithmetic mean intensity of infection in the NGR was similar to Nylsvley, while that at St. Lucia was similar to Delftzyl.

Other common species in the southern KNP were I. tuberculata (2.4-10.1% of adult gastrointestinal nematodes) and S. papillosus (5.6-9.6%). Impalaia tuberculata was the most numerous species at Delftzyl (70.5%) and Nylsvley (36.5%), and second most numerous at St. Lucia (16.9%). The prevalence of adult I. tuberculata was > 80% at Delftzyl, Biyamiti, Skukuza, the NGR and Nylsvley. At the other localities, the prevalence ranged from approximately 40% at St. Lucia and the Tuli Block to 62.5% at Pafuri. The intensity of infection was highest in the NGR, and at Skukuza, Biyamiti, Pafuri, Delftzyl and Nylsvley, and lowest in the Tuli Block and nLP. Strongyloidespapillosus was the second most numerous nematode in the NGR (25.1% of adult gastrointestinal nematodes) and at Pafuri (20.4%). It accounted for 4.3% of the gastrointestinal nematodes at St. Lucia and < 0.1% at Delftzyl and Nylsvley, and was not collected in the Tuli Block or nLP. The prevalence of S. papillosus was 100% at the NGR, > 80% in the KNP, 20% at St. Lucia, and 5% at Delftzyl and Nylsvley. The arithmetic mean intensity of infection in the NGR (5138) was 10fold higher than in the KNP (318-523) and St. Lucia (450), but only four at Nylsvley and six at Delftzyl.

Even though they were widespread, C. fuelleborni, C. hepaticae, L. sabie, O. columbianum and T. falculatus normally accounted for less than 2.5% of the nematode burden. The exceptions were C. fuelleborni, which accounted for 7.0% of the nematodes at Crocodile Bridge in 1980 and 6.3% in the NGR, and L. sabie, which accounted for 5.8% of the nematodes at Delftzyl. The prevalences of C. hepaticae, L. sabie and O. columbianum were > 90% in the NGR, and the arithmetic mean intensities of infection of L. sabie and O. columbianum in the NGR were more than double the intensities in the other localities. The prevalences of C. hepaticae, L. sabie and O. columbianum were 62.5-100.0% in the KNP and Nylsvley. The prevalences of C. hepaticae and O. columbianum were significantly higher in the KNP and Nylsvley than at Delftzyl and the nLP (p > 0.001); L. sabie was not collected in the Tuli Block or St. Lucia, C. hepaticae was not collected at North Tuli, and O. columbianum was not collected in St. Lucia. The logarithmic mean intensity of infection of C. hepaticae did not differ between Skukuza, Biyamiti and Nylsvley, but was significantly lower at South Tuli, Delftzyl and in the nLP (p < 0.001). The logarithmic mean intensity of infection of L. sabie did not differ among localities, while the intensity of infection of O. columbianum was significantly higher at South Tuli and the nLP than at Pafuri, North Tuli, Delftzyl and Nylsvley.

Cooperia fuelleborni and T. falculatus were not collected at Pafuri in 1977/80, but were collected there in 1992/93. Neither species was collected in the Tuli Block, while C. fuelleborni was not collected at Delftzyl and Nylsvley, and T. falculatus was not collected in the nLP or St. Lucia. The prevalence of C. fuelleborni was > 90% in the NGR, and the arithmetic mean intensities of infection of both species were more than double the intensities in the other localities. Outside of the NGR, the prevalence of C. fuelleborni was < 40%. The intensity of infection did not differ between Skukuza, Biyamiti and Crocodile Bridge (p = 0.25), but was higher than at Pafuri, St. Lucia and the nLP. The prevalence of T. falculatus was < 50% at all localities and the logarithmic intensity of infection did not differ among localities (p > 0.2).

Gaigeria pachyscelis, T. thomasi and T. globulosa were collected at the four localities in the KNP and two other localities. The prevalence of G. pachyscelis was > 75% in the southern KNP and NGR, 6.3% at Pafuri and 20% at St. Lucia; it accounted for < 0.4% of the nematodes in the KNP and NGR, and 1.5% at St. Lucia. The prevalence of T. thomasi was > 75% in the southern KNP and 60% at St. Lucia, but only 11% at North Tuli; it was not collected at Pafuri in 1977/80, but was collected there in 1992/93. Trichostrongylus thomasi accounted for approximately 6.5% of the gastrointestinal nematodes in the southern KNP, but < 1.2% at North Tuli and St. Lucia, and at Pafuri in 1992/93. Trichuris globulosa was collected in the KNP, NGR and Delftzyl. The prevalence was > 50% at Skukuza and the NGR, and < 10% at the other localities. The arithmetic mean intensity of infection was 25 at the NGR, but < 10 at the other localities.

Cooperia connochaeti was only collected in the KNP. The prevalence was < 10.6% in the southern KNP, and 50% at Pafuri. It accounted for < 2% of the adult nematodes in the southern KNP and 3.4% at Pafuri. The prevalence of Haemonchus krugeri was 57.1% at Skukuza, 70.2% at Biyamiti, 33.3% at Crocodile Bridge and 20% in the nLP. It accounted for < 2% of the adult nematodes in the southern KNP and 12.5% in the nLP. Haemonchus krugeri was not collected at Pafuri in 1977/80, but was collected there in 1992/93.

The 15 remaining species were collected at three or fewer localities. Nine were relatively uncommon, with prevalences < 50% and accounting for < 1% of the nematode burden. Of the others, C. yoshidai, with a prevalence of 40%, accounted for 10.4% of the nematodes at St. Lucia, while the prevalence of H. placei was 83.3% at Nylsvley where it accounted for 1.5% of the nematodes. The prevalence of H. contortus was 100% at St. Lucia and 60% at Delftzyl, but only 4.3% in the NGR. It was the most numerous nematode at St. Lucia (31.7% of gastrointestinal nematodes), and accounted for 2.4% of the nematodes at Delftzyl. The prevalence of H. bedfordi was 100% in the NGR, but < 10% at Skukuza and Biyamiti. The prevalence of L. schrenki was 60% at St. Lucia, where it accounted for 5.7% of the nematodes, and 26.1% at South Tuli where it accounted for 1.1% of the nematodes. Trichostrongylus axei was relatively common at the NGR and Nylsvley with prevalences of 93.5% and 50% respectively, but accounted for < 2.0% of the adult nematodes; it was not collected at the other localities.

Coinfections

Excluding the NGR and St. Lucia for which individual animal data were not available, the mean number of gastrointestinal nematode species per impala was 7.7 (range 0-14), with a high of 9.8 (range 0-14) in the southern KNP in 1980, and a low of 3.5 (range 0-6) in the Tuli Block and nLP. There was a high degree of coinfection, particularly among the more widespread and numerous species, C. hungi, C. hamiltoni, I. tuberculata, S. papillosus and T. deflexus. However, the prevalence of coinfections was generally similar to that expected based on the product of the individual prevalences.

Trematodes and cestodes

Three taxa of trematodes, paramphistomines, and Fasciola gigantica and Schistosoma mattheei, and three species of cestodes, Monieza benedeni, Monieza expansa and Stilesia hepatica, were collected in the surveys. None were collected in all localities, and with the exception of the paramphistomines, the prevalence was typically < 25% and the intensities of infection were < 25. The prevalence of paramphistomines was > 75% at Biyamiti and the NGR, and the arithmetic mean intensity of infection at Biyamiti was 1 097; paramphistomines were not collected at North Tuli, Delftzyl or the nLP. Schistosoma mattheei was only collected in the southern KNP and F. gigantica was only collected at Nylsvley. The cestode, M. benedeni was collected at Pafuri, the Tuli Block and Delftzyl, while M. expansa was collected at the NGR, Nylsvley and the nLP. Both species were collected at Skukuza and Biyamiti (Table II), but from different individuals. Stilesia hepatica was not collected at North Tuli, Nylsvley or St. Lucia (Table II). There was no association between S. hepatica and C. hepaticae (Kappa = -0.012; p = 0.72).

Effect of drought

The intensity of infection of adult nematodes in the drought-affected impalas in 1982 was significantly higher than in the 1980 matched controls at Skukuza and Crocodile Bridge (p = 0.003), but did not differ at Biyamiti (p = 0.88). The increased intensity of infection at Skukuza and Crocodile Bridge reflected the increased intensities of infection of C. hungi, C. hamiltoni, G. pachyscelis, H. krugeri, I. tuberculata, L. sabie, O. columbianum and T. globulosa, and the increased prevalence of H. krugeri (Table V). The intensities of infection of G. pachyscelis, H. krugeri, I. tuberculata and O. columbianum were also increased in the non-drought-affected impalas. In contrast, there was no increase in the intensities of infection of S. papillosus, T. deflexus, T. falculatus and T. thomasi.

In 1992/93 (Table VI), the intensity of infection of adult nematodes at Skukuza and Crocodile Bridge was less than in 1980 (p < 0.001). The difference reflected declines in the prevalences of C. hepaticae, O. columbianum, S. papillosus, T. deflexus and T. thomasi, and the intensities of infection of C. hungi, C. hamiltoni, C. hepaticae, L. sabie, S. papillosus, T. deflexus and T. thomasi. At Pafuri, the burden of adult nematodes did not differ significantly between 1977/80 and 1992/93 (p = 0.21). In 1992/93, there were increases in the intensity of infection of C. hungi (p = 0.02) and O. columbianum (p = 0.004J, but these were offset by the decrease in the intensity of infection of S. papillosus (p < 0.001). The intensity of infection in 1992/93 did not differ between Skukuza and Pafuri. The intensity of infection was highest at both localities in May-June 1992 and declined in 1993 after the spring/summer rains.

The three most numerous nematodes in the southern KNP in 1980, C. hungi, C. hamiltoni and T. deflexus, accounted for > 66% of the gastrointestinal nematodes. They accounted for approximately the same proportion (> 64%) in the 1982 drought-affected impalas and in 1992/93 at Skukuza and Crocodile Bridge, but only for 58.4% in the drought-affected impalas at Biyamiti in 1982. At Pafuri, C. hungi, C. hamiltoni and T. deflexus accounted for 83.7% of the gastrointestinal nematodes in 1992/93 versus 58.9% in 1980. At all localities, C. hungi accounted for a higher proportion of the gastrointestinal nematodes in 1982 and in 1992/93 than in 1980, while the proportion of T. deflexus declined in the drought years. Agriostomum gorgonis, H. bedfordi and H. vegliai were not collected in the southern KNP in1982, while C. neitzi was collected at Skukuza and Biyamiti (Table V). In 1992/93, C. connochaeti and H. bedfordi, were not collected at Skukuza and A. gorgonis, C. connochaeti and T. globulosa were not collected at Crocodile Bridge, while N. spathiger and T. colubriformis were. At Pafuri, B. trigonocephalum, C. connochaeti, C. hepaticae and T. globulosa were only collected in 1977/80 and C. fuelleborni, H. krugeri, T. falculatus and T. thomasi were only collected in 1992/93.

In 1982, the prevalences and intensities of infection of the trematodes and cestodes did not differ from 1980. In 1992/93, only one (5.9%) impala at Crocodile Bridge was infected with paramphistomines; none were collected at Skukuza or Pafuri. No S. mattheei or M. benedeni were collected in 1992/93, and only three impalas were infected with M. expansa at Crocodile Bridge. The prevalence of S. hepatica was lower in 1992/93 than in 1980 (p = 0.05), but the intensity of infection did not differ.

 

Discussion

The surveys of impala helminths in eastern South Africa and north-eastern Botswana show a mosaic of infections. Ten species of identified nematodes, plus the paramphistomines and the cestode S. hepatica were collected at seven or more of the localities and were considered widely distributed. Nine species of nematodes, the trematode S. mattheei and the cestodes M. benedeni and M. expansa had more restricted distributions and were collected at three to six localities. The remaining 14 species of nematodes and the trematode F. gigantica were only collected at one or two localities.

Helminth species richness was highest in the southern KNP and lowest in the Tuli Block. Five of the six species of nematodes collected at both North and South Tuli, C. hungi, C. hamiltoni, I. tuberculata, O. columbianum and T. deflexus, are widespread species. Other widespread species collected at seven or more localities, such as C. fuelleborni, L. sabie, S. papillosus and T. falculatus, were not collected in the Tuli Block, while C. hepaticae and the cestode S. hepatica were not collected at North Tuli. Among the remaining helminths, G. pachyscelis was only collected in the KNP and KZN; the prevalence was > 75% in the southern KNP and NGR, but only 6% at Pafuri. Trichostrongylus thomasi accounted for 6-9% of the nematodes in the southern KNP, but < 1.2% at North Tuli and St. Lucia. Pneumostrongylus calcaratus was collected in the southern KNP and NGR, and S. mattheei was only collected in the southern KNP.

The nematode burden was highest in the NGR and southern KNP, and lowest in the north and west at North Tuli, Delftzyl and the nLP. This was caused by the lower intensities of infection of C. fuelleborni, C. hungi, C. hamiltoni, I. tuberculata, L. sabie, S. papillosus and T. globulosa, as well as the lower prevalences of C. hepaticae, G. pachyscelis and O. columbianum.

The decreasing helminth species richness, nematode burden, and prevalences and intensities of infection of several nematodes from the southern KNP and the NGR to the Tuli Block, Delftzyl and nLP appear to be related to annual rainfall, which ranged from 900 mm per annum in the NGR to approximately 350 mm per annum in the Tuli Block and nLP. Drier conditions will reduce the environmental survival of the free-living stages of directly transmitted nematodes, and the survival and distribution of the intermediate hosts of indirectly transmitted helminths, such as P. calcaratus and the trematodes and cestodes.

South Tuli was an anomaly in the relationship between intensity of infection and rainfall, primarily because of the high intensity of infection in 1986. There are two possible explanations. First, 1986 was the second of two years of below average rainfall, and the higher intensity of infection in 1986 than in 1988 may reflect the short-term effect of drought and increase in the intensity of infection of gastrointestinal nematodes as seen in the drought-affected impalas in the southern KNP in 1982. The second explanation may be the age-sex distribution of the 1986 sample, in which there was a mix of sexes from May to August, but only females in October and November. At Skukuza and Biyamiti in 1980, there was a marked increase in the intensity of infection of nematodes in adult female impalas relative to the other age-sex classes from November to December (Horak et al. 2023). This was attributed to a periparturient relaxation of resistance in the females.

The 10 most widespread species of nematodes accounted for > 90% of the nematodes in the KNP, Tuli Block and at Delftzyl, with T. deflexus, C. hungi and C. hamiltoni the most numerous species in the southern KNP and Tuli Block. These three species were also common at Pafuri, and C. hungi and C. hamiltoni were common at Delftzyl and Nylsvley. In the nLP, C. hungi was the most numerous species. Impalaia tuberculata was the most numerous species at Delftzyl and Nylsvley, and the second most numerous species at St. Lucia and the nLP, while S. papillosus was the second most numerous at Pafuri and the NGR. Even though they were widespread, C. hepaticae, L. sabie, O. columbianum and T. falculatus seldom accounted for more than 2.5% of the nematode burden.

Trichostrongylus colubriformis was the most numerous nematode in the NGR and second most numerous at Nylsvley. It appears to replace T. deflexus. However, the collections in the NGR and at Nylsvley were from 1973 to 1976 (Anderson 1983; Horak 1978) and T. deflexus, which closely resembles T. colubriformis, was not described until 1989 (Boomker & Reinecke 1989).

Cooperia hungi was also not collected in the NGR, although Anderson (1983) reported it from the Hluhluwe Game Reserve in KZN, and it was collected at St. Lucia. The prevalence of C. hungi was > 75% at most localities, and it accounted for 13.6-59.3% of the gastrointestinal nematodes; it was the most numerous nematode at South Tuli in 1986 and in the nLP. At St. Lucia, the prevalence was 40% and it accounted for < 2% of the nematodes. As noted above, there was an increased intensity of infection of C. hungi in the drought-affected impalas in 1982. In 1992/93, the intensity of infection was increased at Pafuri, and even though the intensity of infection declined at Skukuza and Crocodile Bridge, the decline was less than for other species and C. hungi accounted for a higher proportion of the gastrointestinal nematodes. Interestingly, Boomker et al. (1991) did not collect any C. hungi from nyalas, Tragelaphus angasii, in north-eastern Natal in 1983/84 at the end of a wet cycle, but Boomker et al. (1996) reported an overall prevalence of 29.3% and arithmetic mean intensity of infection of 186 in 1991 at the end of a dry cycle. Thus, whereas for many nematodes the distribution and burden appear to be limited by low rainfall, C. hungi may be adapted to drier conditions.

St. Lucia was the most dissimilar locality, with the lowest proportion of widespread species and highest proportion of unique species. Haemonchus contortus was the most numerous nematode, followed by I. tuberculata and C. yoshidai. The intensities of infection of the widespread nematodes, C. hungi and C. hamiltoni, were lower than at most other localities, and L. sabie, O. columbianum, T. deflexus and T. falculatus, were not collected there, although Boomker et al. (1989b) list Oesophagostomum sp. in impalas, and O. columbianum was collected from reedbuck, Redunca arundinum, in the reserve. Several of the helminths collected at St. Lucia, C. yoshidai, D. viviparus, T. angistris, T. instabilis and the genus Ostertagia, were not collected at the other localities, or were only collected at one or two, i.e. H. contortus and L. schrenki. Haemonchus contortus, C. yoshidai, D. viviparus and L. schrenki were common parasites of reedbuck in the reserve (Boomker et al. 1989b).

Host assemblage is another factor that may influence helminth species richness and burden. In a comparative analysis of the gastrointestinal nematode burdens of herbivores in the south-central KNP (Horak et al. 2021), impalas had the highest nematode burden and species richness of the antelope (impalas, blue wildebeest, Connochaetes taurinus, and kudus, Tragelaphus strepsiceros). Three nematodes, C. hamiltoni, H. krugeri and L. sabie were only collected from impalas. To this list we may add C. hepaticae, which was not collected from the other antelope (Boomker et al. 1989a; Horak et al. 1983) and other hosts, warthogs, Phacochoerus africanus (as Phacochoerus aethiopicus), (Horak et al. 1988) and scrub hares, Lepus saxatilis (Boomker et al. 1997). Impalas were also the main hosts of C. hungi, I. tuberculata and S. papillosus, while the main hosts of T. deflexus were impalas and scrub hares. With the exception of H. krugeri which was only collected in the KNP and nLP, the nematodes of which impalas were the main hosts in the southern KNP are widespread and usually among the most numerous species.

Amongst the antelope (Horak et al. 2021), three genera of nematodes, Cooperia, Cooperioides and Haemonchus, exhibited host specificity, with C. hungi, C. hamiltoni, C. hepaticae and H. krugeri associated with impalas, Cooperia acutispiculum, C. neitzi and H. vegliai associated with kudus, and C. connochaeti and H. bedfordi with wildebeest. Cooperia connochaeti, H. bedfordi and H. vegliai were also collected from impalas in 1980, and C. neitzi was collected from impalas in the 1982 drought; none were collected in 1992/93. With the exception of C. connochaeti at Pafuri in 1980, the prevalence of these species was < 10%, suggesting that they were incidental infections.

A number of helminths, F. gigantica, H. contortus, H. placei, G. pulchrum and T. axei, collected from impalas at the NGR or Nylsvley were not collected in the KNP, or were rarely collected, i.e. T. colubriformis. All of these are parasites of domestic stock (Reinecke 1983). The NGR had been converted from a cattle ranch to a game farm approximately nine years prior to Anderson's (1983) collections, and the Nylsvley Nature Reserve had a herd of cattle (Horak 1978). Fasciola gigantica was also collected from an impala in north-eastern Eswatini in a reserve that had previously been a cattle ranch (Gallivan et al. 1996). Haemonchus contortus was collected from 60% of the impalas at Delftzyl and T. colubriformis was collected from 15%. Both species were also parasites of indigenous goats on the farm, with prevalences of 92% for H. contortus and 27% for T. colubriformis (Boomker et al. 1994).

Horak et al. (2021) postulated that because impalas are intermediate feeders they would be exposed to nematodes infecting both browsers (kudus) and grazers (wildebeest). The widespread distribution of impalas throughout eastern South Africa also exposes them to a range of helminths infecting other antelope and domestic hosts. Thus, while impalas are primary hosts to several helminths, they are also infected by helminths that infect several other species and contribute to the helminth species richness of impalas.

Effect of drought

The response to drought conditions at Skukuza and Crocodile Bridge differed between 1982 and 1992/93, with an increase in nematode burdens in 1982 and a decrease in 1992/93. These patterns were similar to those reported for ticks collected at the same time (Horak et al. 1995, 2003). Horak et al. (1995, 2003) attributed the differences in tick response to differences in the droughts and impala populations. The collections in the 1982 drought were made at the end of the dry season following a period of low rainfall beginning in February 1982. This was preceded by a period of above average rainfall from 1971 to 1981 (Fig. 2), and the impala population in the Skukuza area was approximately 4 500. In contrast, the 1992/93 collections began at the end of the 1991/92 drought and encompassed a year of above average rainfall in 1992/93. The collections followed a period of below average rainfall from 1982 to 1992, and the impala population in the Skukuza area was approximately 1 000.

The differences in responses suggest both an acute and longterm response to drought. The acute response was an increase in nematode burdens and the intensities of infection of several nematode species, C. hungi, C. hamiltoni, G. pachyscelis, H. krugeri, I. tuberculata, L. sabie, O. columbianum and T. globulosa. The increased nematode burdens in the non-drought affected impalas support the hypothesis that the drought was a factor. However, whether the increased nematode burden contributed to the poor condition of the drought-affected impalas, or whether the nematode burden was a result of their condition cannot be determined.

In 1992/93, the decline in nematode populations at Skukuza and Crocodile Bridge occurred in several species, C. hungi, C. hamiltoni, C. hepaticae, L. sabie, O. columbianum, S. papillosus, T. deflexus, T. thomasi and T. globulosa. For some, C. hamiltoni, C. hepaticae, L. sabie, S. papillosus and T. globulosa, the overall prevalence and/or intensity of infection exhibited a decrease from the higher rainfall localities in the southern KNP and KZN to the lower rainfall localities in the Tuli block and nLP. The distributions of other species such as C. fuelleborni, G. pachyscelis and T. thomasi were restricted primarily in the southern KNP and KZN. While C. hungi, C. hamiltoni, C. hepaticae, G. pachyscelis and L. sabie are primarily parasites of impalas, the other nematodes, S. papillosus, T. deflexus, T. falculatus and T. thomasi, infect a range of hosts (Horak et al. 2021). The decline in impala populations from 1982 to 1992/93 coincided with the population declines of several ungulate species in the KNP beginning in the mid-1980s (Ogutu & Owen Smith 2005). Thus, the helminth burden of impalas may be affected, not just by the alternate hosts available, but also by both the population density of the impalas and the alternate hosts.

In contrast to Skukuza, there was little or no difference in the nematode burdens relative to 1980 at Biyamiti in 1982, or relative to 1977/80 at Pafuri in 1992/93. The lack of a statistically significant difference between the drought-affected impalas at Biyamiti in 1982 and 1980 controls may be the result of small sample sizes and high variance within the samples. While there wasn't a difference between years in the burdens at Pafuri, there was a shift in species as C. connochaeti, C. hepaticae and T. globulosa were not collected in 1992/93 and there was a decrease in the intensity of infection of S. papillosus (p < 0.001). These were largely replaced by C. hungi, which may be more tolerant of drier conditions.

Acknowledgements

We are indebted to SANParks for placing the animals as well as their staff and facilities in the Kruger National Park at our disposal and to Dr V de Vos, who facilitated the project in the Park. We gratefully acknowledge the assistance of Prof J Boomker with helminth collection and identification. We thank Messrs C Cheney, J Sithole and BD de Klerk for assistance with processing the carcasses for the recovery of parasites, and Miss ML Horak and Messrs AC Uys, DG Booyse and R Watermeyer, who assisted in the recovery of helminths from the processed material. This research was funded by the Faculty of Veterinary Science, University of Pretoria, SANParks, the National Research Foundation and Bayer Animal Health. The Department of Agriculture and Water Supply funded the project at Delftzyl and placed the impalas there at our disposal.

Conflict of interest

The authors declare they have no conflicts of interest that are directly or indirectly related to the research.

Funding source

This research was funded by the Faculty of Veterinary Science, University of Pretoria, SANParks, and Bayer Animal Health.

Compliance with ethical guidelines

The authors declare that this submission is in accordance with the principles laid down by the Responsible Research Publication Position Statements as developed at the 2nd World Conference on Research Integrity in Singapore, 2010.

Ethical approval

All applicable institutional, national and international guidelines for the care and use of animals were followed.

ORCID

IG Horak https://orcid.org/0000-0002-2200-6126

K Junker https://orcid.org/0000-0001-6650-1201

GJ Gallivan https://orcid.org/0000-0002-2096-5657

LEO Braack https://orcid.org/0000-0002-5286-5052

 

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Correspondence:
K Junker
Email: junkerk@arc.agric.za