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Parasitological monitoring of European bison (Bison bonasus) from three forests of north-eastern Poland between 2014 and 2016

Michał K. Krzysiak
Michał K. Krzysiak
, 
Aleksander W. Demiaszkiewicz
Aleksander W. Demiaszkiewicz
, 
Magdalena Larska
Magdalena Larska
, 
Jarosław Tomana
Jarosław Tomana
 oraz 
Krzysztof Anusz
Krzysztof Anusz
   | 24 mar 2020
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Data publikacji: 24 mar 2020
Zakres stron: 103 - 110
Otrzymano: 03 wrz 2019
Przyjęty: 02 mar 2020
DOI: https://doi.org/10.2478/jvetres-2020-0022
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© 2020 M.K. Krzysiak et al. published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Fig. 1

Box plot of numbers of gastro-intestinal nematode eggs (black), Eimeria spp. oocysts (dark grey), Fasciola hepatica (light grey), and Dictyocaulus viviparus eggs (white) broken down by origin (A) and season (B). Boxes show the median and upper and lower quartiles, while the whiskers illustrate the data range. The additional dot, square, or diamond points stand for outliers. The statistically significant differences were verified using the Kruskal–Wallis test and are indicated with * for P between 0.05 and 0.001 and ** for P < 0.001
Box plot of numbers of gastro-intestinal nematode eggs (black), Eimeria spp. oocysts (dark grey), Fasciola hepatica (light grey), and Dictyocaulus viviparus eggs (white) broken down by origin (A) and season (B). Boxes show the median and upper and lower quartiles, while the whiskers illustrate the data range. The additional dot, square, or diamond points stand for outliers. The statistically significant differences were verified using the Kruskal–Wallis test and are indicated with * for P between 0.05 and 0.001 and ** for P < 0.001

Cross-correlations between the explanatory variables and outcomes – prevalence and intensity of invasion

Origin Season Trichostrongylidae Aonchotheca sp. Nematodirus spp. Strongyloides spp. Trichuris sp. Moniezia spp. Eimeria spp. Fasciola hepatica Dictyocaulus viviparus
Origin 1 - 27.1

– P <0.001;

 68.5

– P <0.001;

 33.2

– P <0.001;

 7.3 22.9

– P <0.001;

 12.0

– P value between 0.05 and 0.001;

 92.3

– P <0.001;

 37.2

– P <0.001;

 86.4

– P <0.001;
Season 72.1

– P <0.001;

 1 102.1

– P <0.001;

 4.5 6.0 1.9 12.0

– P value between 0.05 and 0.001;

 15.0

– P <0.001;

 3.2 13.4

– P value between 0.05 and 0.001;

 56.4

– P <0.001;
Trichostron- gylidae 0.73 7.9

– P value between 0.05 and 0.001;

 1 0.15

– P value between 0.05 and 0.001;

 0.22

– P <0.001;

 −0.09 0.29

– P <0.001;

 0.27

– P <0.001;

 0.13

– P value between 0.05 and 0.001;

 0.25

– P <0.001;

 0.38

– P <0.001;

 Intensity of invasion (number of eggs/oocysts/larvae)
Aonchotheca sp. 74.4

– P <0.001;

 3.2 5.8

– P value between 0.05 and 0.001;

 1 0.11 −0.07 0.10 0.07 0.38

– P <0.001;

 0.16

– P value between 0.05 and 0.001;

 0.15

– P value between 0.05 and 0.001;
Nematodirus spp. 32.6

– P <0.001;

 5.9

– P value between 0.05 and 0.001;

 1.6 7.0

– P value between 0.05 and 0.001;

 1 −0.02 0.46

– P <0.001;

 0.35

– P <0.001;

 0.16

– P value between 0.05 and 0.001;

 0.22

– P <0.001;

 0.26

– P <0.001;
Strongyloides spp. 7.3 2.0 0.2 2.1 0.2 1 −0.03 −0.03 −0.06 −0.08 −0.06
Trichuris sp. 22.5

– P <0.001;

 11.9

– P value between 0.05 and 0.001;

 1.6 4.1

– P value between 0.05 and 0.001;

 74.9

– P <0.001;

 0.2 1 0.47

– P <0.001;

 0.15

– P value between 0.05 and 0.001;

 0.22

– P <0.001;

 0.29

– P <0.001;
Moniezia spp. 11.9

– P value between 0.05 and 0.001;

 14.7

– P value between 0.05 and 0.001;

 1.9 0.8 41.6

– P <0.001;

 0.3 71.2

– P <0.001;

 1 0.09 0.15

– P value between 0.05 and 0.001;

 0.20

– P <0.001;
Eimeria spp. 7.4 12.5

– P value between 0.05 and 0.001;

 0.06 35.6

– P <0.001;

 5.8

– P value between 0.05 and 0.001;

 1.1 4.5

– P value between 0.05 and 0.001;

 4.7

– P value between 0.05 and 0.001;

 1 0.01 0.04
Fasciola hepatica 27.7

– P <0.001;

 3.0 2.3 3.7

– P value between 0.05 and 0.001;

 5.1

– P value between 0.05 and 0.001;

 1.2 5.6

– P value between 0.05 and 0.001;

 2.6 1.0 1 0.33

– P <0.001;
Dictyocaulus viviparus 81.7

– P <0.001;

 59.2

– P <0.001;

 0.6 11.7

– P value between 0.05 and 0.001;

 16.0

– P <0.001;

 1.2 22.1

– P <0.001;

 9.6

– P value between 0.05 and 0.001;

 2.3 18.2

– P <0.001;

 1
Prevalence (presence/absence of parasite)

The numbers of different gastro-intestinal nematodes, Fasciola hepatica eggs, Dictyocaulus viviparus larvae, and Eimeria spp. oocysts and the parasite prevalence in European bison from the Białowieża Forest (n = 139) and its neighbouring area (n = 96) and the Knyszyńska (n = 107) and Borecka (n = 26) Forests collected in the autumns of 2014 and 2015 (n = 223), winter 2016 (n = 51), and spring 2015 (n = 94)

Parasite species (adult gastro-intestinal nematodes except where noted) Variables
Origin
 Season
Białowieża Forest (BiF) BiF neighbouring area Knyszyńska Forest Borecka Forest Autumn Winter Spring
Trichostrongylidae n

– mean of egg numbers per 3 g of faeces;

 37.9 98.2 25.1 14.1 14.2 43 131.9
(range) (1–1150) (1–1196) (1–305) (1–45) (1–98) (1–448) (1–1196)
%

– standard deviation;

 95.7 93.7 94.4 92.3 92 100 98
(SD

– % mean prevalence;

)		 (20.4) (24.3) (23.1) (27.2) (27.3) (0) (14.5)
Aonchotheca spp. n

– mean of egg numbers per 3 g of faeces;

 5.3 4.2 1.3 6.2 3.8 2 3.1
(range) (1–82) (1–58) (1–8) (1–28) (1–82) (1–20) (1–79)
%

– standard deviation;

 54.7 59.4 7.4 34.6 43.5 43.1 32.9
(SD

– % mean prevalence;

)		 (50) (49.4) (26.4) (48.5) –49.7 (50) (47.2)
Nematodirus spp. n

– mean of egg numbers per 3 g of faeces;

 0.06 1.1 0.02 0.1 1 0.4
(range) (1–4) (1–24) (1–1) 0 (1–13) (1–24) (1–10)
%

– standard deviation;

 3.6 19.8 1.9 4.5 9.8 11.7
(SD

– % mean prevalence;

)		 (18.7) (40) (13.6) 0 (20.7) (30) (32.3)
Strongyloides spp. n

– mean of egg numbers per 3 g of faeces;

 0.1 0.05
(range) 0 0 (1–5) 0 (1–5) 0 0
%

– standard deviation;

 2.8 1.3
(SD

– % mean prevalence;

)		 0 0 (16.6) 0 (11.5) 0 0
Trichuris spp. n

– mean of egg numbers per 3 g of faeces;

 2.1 19.8 0.6 1.7 10.3 14.3
(range) (1–152) (1–305) (1–61) 0 (1–136) (1–249) (1–305)
%

– standard deviation;

 5.8 17.7 1.9 3.6 11.8 13.8
(SD

– % mean prevalence;

)		 (23.3) (38.4) (13.6) 0 (18.6) (32.5) (34.7)
Moniezia spp. n

– mean of egg numbers per 3 g of faeces;

 1.7 14.3 4.5 2.1 6.5 14
(range) (1–142) (1–304) (1–267) 0 (1–267) (1–142) (0–304)
%

– standard deviation;

 8.6 15.6 3.7 4 17.6 13.8
(SD

– % mean prevalence;

)		 (28.2) (36.5) (19.1) 0 (19.7) (38.5) (34.7)
Eimeria spp. (oocysts) n

– mean of oocyst numbers per 5 g of faeces

 45.4 99.2 10.8 160.6 65.9 27.5 53.8
(range) (1–748) (1–5072) (1–557) (1–1914) (1–5072) (1–391) (1–1917)
%

– mean of oocyst numbers per 5 g of faeces

 74.8 77.1 25.2 96.1 56 82.3 65.9
(SD

– % mean prevalence;

)		 (43.5) (42.2) (43.6) (19.6) (49.7) (38.5) (47.6)
Fasciola hepatica (eggs) n

– mean of egg numbers per 3 g of faeces;

 8.7 8.7 2.4 5.3 3.5 18.3 7.5
(range) (1–403) (1–63) (1–22) (1–62) (1–63) (1–403) (1–38)
%

– standard deviation;

 69.1 78.1 53.3 30.8 62.3 58.8 71.3
(SD

– % mean prevalence;

)		 (46.4) (41.6) (50.1) (47.1) (48.5) (49.7) (45.5)
Dictyocaulus viviparus (larvae) n

– mean of egg numbers per 3 g of faeces;

 5 49.8 28.4 6 20.7 40.6
(range) (1–173) (1–856) 0 (1–276) (1–276) (1–176) (1–856)
%

– standard deviation;

 26.6 55.2 46.1 14.4 33.3 56.4
(SD

– % mean prevalence;

)		 (44.3) (50) 0 (50.8) (35.1) (47.6) (49.8)

Mixed-effects generalised linear model (GLM) coefficients for the effects of season and origin on the probability of European bison of being infected with individual parasites

Origin (forest)
 Season
BiF BiFneighbouringarea KnF BoF Autumn Winter Spring Intercept
Aonchotheca sp.
Coefficient βStandard errorz statisticP >|z| 0.22 0.29 0.77 0.44 −2.96 0.42 −7.01 <0.001 −0.79 0.47 −1.68 0.09 −0.90 0.34 −2.65 0.008 −0.84 0.30 −2.78 0.005 0.58 0.21 2.73 0.006
Trichuris sp.
Coefficient βStandard errorz statisticP >|z| 1.20 0.49 2.44 0.02 −0.95 0.84 −1.13 0.26 0 – – – 1.13 0.60 1.88 0.06 1.30 0.49 2.68 0.007 −3.47 0.49 −6.96 <0.001
Dictyocaulus viviparus
Coefficient βStandard errorz statisticP >|z| 1.05 0.32 3.26 0.001 0 – – – 0.21 0.53 0.40 0.69 0.75 0.38 1.98 0.05 2.29 0.36 6.35 <0.001 −1.67 0.27 −6.23 <0.001

The numbers of faecal samples collected by location and season

Season Location
Borecka Forest Knyszyńska Forest Białowieża Forest BiF neighbouring region Total
Autumn 2014 12 18 78 50 158
Autumn 2015 0 65 0 0 65
Spring 2015 14 24 20 36 94
Winter 2016 0 0 41 10 51
Total 26 107 139 96 368

Mixed-effect generalised linear model (GLM) coefficients for the effects of season and origin on the intensity of individual parasite invasion in European bison

Origin (forest)
 Season
BiF BiFneighbouringarea KnF BoF Autumn Winter Spring Intercept
Trichostrongylidae
Coefficient βStandard errorz statisticP >|z| 0.50 0.02 27.2 <0.001 −0.48 0.02 −19.0 <0.001 −1.7 0.05 −30.8 <0.001 0.95 0.03 33.11 <0.001 2.16 0.02 106.4 <0.001 2.69 0.02 127.3 <0.001
Aonchotheca sp.
Coefficient βStandard errorz statisticP >|z| −0.34 0.06 −5.38 <0.001 −3.10 0.18 −17.14 <0.001 −0.75 0.12 −6.11 <0.001 −1.18 0.10 −11.20 <0.001 −0.23 0.07 −3.30 <0.001 1.94 0.04 47.9 <0.001
Nematodirus spp.
Coefficient βStandard errorz statisticP >|z| 3.33 0.35 9.44 <0.001 −0.25 0.80 −0.32 0.75 −12.55 614.7 −0.02 0.98 2.05 0.22 9.00 <0.001 0.53 0.24 2.20 0.03 −3.87 0.38 −10.21 <0.001
Trichuris sp.
Coefficient βStandard errorz statisticP >|z| 2.18 0.06 33.27 <0.001 −0.82 0.14 −5.93 <0.001 −16.49 481.7 −0.03 0.97 1.76 0.07 25.72 <0.001 1.71 0.06 29.45 <0.001 −0.36 0.08 −4.69 <0.001
Moniezia spp.
Coefficient βStandard errorz statisticP >|z| 1.95 0.07 26.61 <0.001 1.21 0.08 14.23 <0.001 −16.1 414.4 −0.04 0.97 1.51 0.08 19.60 <0.001 1.74 0.06 31.57 <0.001 −0.43 0.08 −5.34 <0.001
Eimeria spp.
Coefficient βStandard errorz statisticP >|z| 0.76 0.02 45.62 <0.001 −1.62 0.03 −50.10 <0.001 1.25 0.02 60.05 <0.001 −0.99 0.03 −34.66 <0.001 −0.59 0.02 −35.12 <0.001 4.10 0.01 305.10 <0.001
Fasciola hepatica
Coefficient βStandard errorz statisticP>|z| 0.20 0.05 4.21 <0.001 −0.77 0.07 −10.30 <0.001 −0.16 0.09 −1.71 0.09 1.42 0.05 27.33 <0.001 0.65 0.05 12.27 <0.001 1.44 0.04 32.17 <0.001
Dictyocaulus viviparus
Coefficient βStandard errorz statisticP >|z| 2.21 0.04 51.89 <0.001 −19.31 770.34 −0.03 0.98 1.54 0.06 27.65 <0.001 1.26 0.04 29.94 <0.001 1.40 0.03 43.70 <0.001 0.82 0.04 18.00 <0.001
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