Leucocytozoon spp

Wiegmann, Anja, Springer, Andrea, Rinaud, Tony, Ottensmann, Meinolf, Legler, Marko, Krüger, Oliver, Fehr, Michael, Chakarov, Nayden & Strube, Christina, 2021, The prevalence of Leucocytozoon spp. in nestlings of three wild raptor species including implications on haematological and blood chemistry values, International Journal for Parasitology: Parasites and Wildlife 16, pp. 236-243 : 238-239

3.1. Prevalence of Leucocytozoon spp . in raptor nestlings

In total, 528 samples were screened for Leucocytozoon spp ., comprising 464 common buzzards, 46 red kites and 18 northern goshawks. Leucocytozoon infections were detected in 51.9% (274/528) of all raptor nestlings. Prevalence in common buzzards was 54.9% (255/ 464), in red kites 32.6% (15/46) and in northern goshawk 22.2% (4/18) ( Fig. 1 ). Among the 274 infected nestlings, 21.5% showed a low, 27.4% a medium and 51.1% a high infection intensity. Regarding the onset of infection, there was a steep increase in the first half of the nesting period, and by the end of this first half, more than 50% of the tested individuals were infected ( Fig. 2 ).

Leucocytozoon prevalence in goshawks and red kites was significantly lower than in common buzzards (GLMM, P = 0.034 and P = 0.013, respectively, Table 1). Furthermore, the likelihood of infection increased with the standardised age (P = 0.027, Table 1). Among the 447 common buzzards for which these variables were available, the effect of standardised age was similar in magnitude, but did not reach statistical significance (P = 0.077). Furthermore, the likelihood of infection was not explained by sex or plumage morph (Supplementary Table 1).

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3.2. Effects of Leucocytozoon infection on haematological and blood chemistry parameters

Eighty-seven samples were analysed for 12 haematological and 10 blood chemistry parameters. Of the 87 individuals, a total of 48 chicks were identified as male and 39 as female. Among common buzzards, 30 were male and 20 female, among red kites 15 were male and 14 female, and among goshawks 3 were male and 5 female. Obtained haematological values are presented in Table 2, and blood chemistry values in Table 3. Due to the low levels of variation in GLDH and basophil values, these were not considered in this analysis .

Overall, there was a considerable overlap in most blood parameter values between infected and uninfected nestlings ( Table 3). However, the LDA indicated that the blood profiles differed slightly between uninfected and infected nestlings ( Fig. 3 ). The variance-covariance matrix was homogeneous and the multivariate distribution of the variables followed a normal distribution. An error rate of 30.1% [standard deviation (SD): 0.78] was estimated in predicting infection status (infected or uninfected) in seven subsets randomly selected from the complete dataset, using a cross validation method.

Based on the LDA result, linear models were employed to quantify the influence of infection on nine predominantly affected blood parameters (lymphocytes, monocytes, heterophils, eosinophils, AST, BA, BuChE, LDH, AP), taking bird species, sex and age into consideration. Significant differences in blood parameter values with respect to infection status were observed for seven parameters ( Table 4, Supplementary Table 2). Infection was significantly associated with elevated heterophil, AST, LDH, BA and BuChE, but decreased lymphocyte and monocyte values. Regarding these seven parameters, all were within the species-specific standard range, with the exception of LDH in northern goshawks, where the values of uninfected also deviated from references ( Chitty and Lierz, 2008; Gelli et al., 2009; Hanauska-Brown et al., 2003; Hernandez et al., 1990; Stout et al., 2010).

3.3. The influence of sex, species and age on blood parameters of raptor nestlings

Neither infection status nor haematological and blood chemistry parameters differed between male and female nestlings in any of the three raptor species ( Table 4). In contrast, species differed significantly regarding all haematological parameters, except lymphocyte proportion. The heterophil fraction was approximately 28% higher in red kites compared to common buzzards (Supplementary Table 2). Red kites also had higher BA values, whereas their eosinophil and BuChE levels were lower than in both common buzzards and northern goshawks. Moreover, significantly lower proportions of monocytes were observed in northern goshawk than in the other two species, while significant differences in AST, AP and LDH levels appeared between all examined species. In addition, age had a significant positive effect on AST, AP and eosinophil counts.

Furthermore, significant interaction effects were detected. In older raptor chicks, the effect of Leucocytozoon infections on AST was weaker than in younger individuals. Also, the difference in monocyte levels between northern goshawks and common buzzards decreased with age in both infected and uninfected nestlings. In red kites, the effect of Leucocytozoon infections on LDH was smaller compared to buzzards. No apparent sex-infection interactions appeared to explain any additional variation in blood parameters.

Figures

Fig. 1. Prevalence of Leucozytozoon spp. infection in nestlings of common buzzards (Buteo buteo), red kites (Milvus milvus) and northern goshawks (Accipiter gentilis). Asterisks refer to P-values ≤0.05, determined by GLMM. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2. Proportion of infected individuals of common buzzard (Buteo buteo), red kite (Milvus milvus) and northern goshawk (Accipiter gentilis) nestlings (n = 528) in relation to the proportion of the nestling period, determined by age and the species-specific average nestling duration. Calculated nestling periods were grouped into steps of ten percent (0.2–0.9). Each step represents the proportion of all individuals examined within this period. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 3. Results of linear discriminant analysis (LDA) comparing 15 selected blood parameters between uninfected and infected raptor nestlings. a) Distribution of the LDA according to uninfected and infected nestlings. b) Correlation plot of the first axis of the 15 selected variables.