Oral disease is linked to low nestling condition and brood size in a raptor species living in a highly modified environment

Abstract

Anthropogenic stressors can favor the occurrence of noninfectious disease that can be worsened by the impact of opportunistic pathogens, making the epizootiology of environmental diseases difficult to unravel. The incidence and impact of oral lesions in nestlings of a facultative scavenger species, the black kite Milvus migrans, were examined over seven breeding seasons in the highly degraded environment close to Madrid, Spain. We found an overall prevalence of 31% of nestlings with oral lesions, with no clear spatial pattern in nests with affected and unaffected individuals. The occurrence and number of oral lesions were negatively associated with nestling body condition and brood size. Broods, where all siblings had oral lesions, were smaller than those where some or all siblings were apparently healthy, suggesting that oral disease could be causing nestling mortality and, consequently, brood size reduction. In turn, nestling body condition was negatively affected by lesion occurrence, brood size, and laying date. Although these relationships were bidirectional, piecewise structural equation modeling analyses showed a greater negative effect of body condition on lesion occurrence than vice versa, indicating that nestlings in poorer body condition were more likely to develop oral lesions (which could contribute to aggravate their state of deterioration) than those in better condition. Nestlings from small broods were also more likely to have oral disease (directly or indirectly through their lower body condition) than nestlings from large broods. Nestlings that hatched last in the broods showed greater development stress than those that hatched first. Anthropogenic stressors could trigger poor body condition, and contribute to microbiota dysbiosis-related diseases. Although further research is needed to determine the consequences for the long-term fitness of individuals, actions should be taken to mitigate adverse conditions that may favor the appearance of environmental diseases associated with peri-urban areas, given their rapid expansion over natural areas.

Keywords: body condition; breeding success; developmental stress; environmental disease; habitat degradation; opportunistic pathogens; pollution; raptor.

Figure 1.

(A) Location of the study area in Madrid, Central Spain. (B) Spatial distribution of sampled nests where nestling black kites were examined to determine the occurrence of oral lesions. Red and blue circles represent nests with nestlings with and without lesions, respectively. The size of circles represent the number of years (1–4) that each nest was sampled, while sections within each circle represent the number of years with diseased and undiseased nestlings. Yellow stars indicate the location of landfills. (C) Nestling black kites.

Figure 2.

Mean (± 95% CI) interannual and total prevalence of lesions (A), and number of lesions (B) in nestling black kites; sample size is shown above the bars. (C) Number of nestlings affected by different number of lesions.

Figure 3.

Effects of individual body condition (A) and number of siblings in a brood (brood size) (B) on the probability of occurrence of lesions in nestling black kites. Number of broods within each category (1–4 nestlings) is shown in brackets.

Figure 4.

Mean brood size (± 95% CI) in nests where no nestlings had apparent lesions (all −), some nestlings had lesions but others did not (+/-) and all nestlings were affected (all +).

Figure 5.

SEM exploring the relationships between the occurrence of lesions, body condition, and developmental stress and individual age, laying date, order in a brood, brood size, and distance to the nearest dump. Arrows represent unidirectional relationships among variables. Black and gray arrows denote significant and nonsignificant paths, respectively (P ≥ 0.05). The thickness of the significant paths has been scaled based on the magnitude of the standardized regression coefficient (Supplementary Table S2). R² for component models are given in the boxes of response variables.