Population structure of the soft tick Ornithodoros maritimus and its associated infectious agents within a colony of its seabird host Larus michahellis

Abstract

The epidemiology of vector-borne zoonoses depends on the movement of both hosts and vectors, which can differ greatly in intensity across spatial scales. Because of their life history traits and small size, vector dispersal may be frequent, but limited in distance. However, little information is available on vector movement patterns at local spatial scales, and particularly for ticks, transmitting the greatest diversity of recognized infectious agents. To test the degree to which ticks can disperse and disseminate pathogens at local scales, we investigated the temporal dynamics and population structure of the soft tick Ornithodoros maritimus within a colony of its seabird host, the Yellow-legged gull Larus michahellis. Ticks were repeatedly sampled at a series of nests during the host breeding season. In half of the nests, ticks were collected (removal sampling), in the other half, ticks were counted and returned to the nest. A subsample of ticks was screened for known bacteria, viruses and parasites using a high throughput real-time PCR system to examine their distribution within the colony. The results indicate a temporal dynamic in the presence of tick life stages over the season, with the simultaneous appearance of juvenile ticks and hatched chicks, but no among-nest spatial structure in tick abundance. Removal sampling significantly reduced tick numbers, but only from the fourth visit onward. Seven bacterial isolates, one parasite species and one viral isolate were detected but no spatial structure in their presence within the colony was found. These results suggest weak isolation among nests and that tick dispersal is likely frequent enough to quickly recolonize locally-emptied patches and disseminate pathogens across the colony. Vector-mediated movements at local scales may therefore play a key role in pathogen emergence and needs to be considered in conjunction with host movements for predicting pathogen circulation and for establishing effective control strategies.

Keywords: Argasidae; Dispersal; Epidemiology; Within-nest dynamics.

Graphical abstract

Fig. 1

Map showing the position of the 30 tracked nests on Carteau Island, in the Camargue region of France (represented by the red point on the bottom right map). Orange points represent the 15 nests in which ticks were counted and released. The green points are those nests where all ticks were counted and collected. Stars within the points represent the nests in which ticks were used for the screening of infectious agents. Boxes indicate the number of ticks screened and the detected infectious agents: Ana: Anaplasma spp.; Bab: Babesia spp.; Bar: Bartonella spp.; Bor: Borrelia spp.; Cox: Coxiella-like symbiont; Fra: Francisella-like symbiont; Ri: Rickettsia helvetica; Ri-like: Rickettsia-like symbiont. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Histogram presenting the mean number of ticks observed in all nests over time. Bars represent mean standard errors of the total number of ticks.

Fig. 3

Boxplot representations of tick numbers in counted and collected nests over time: a, females only; b, males only; c, nymphs. The box shows the median as a line across the middle and the quartiles (25th and 75th percentiles) at either end. Extremities represent the minimal and maximal values and circles represent outliers.

Fig. 4

Spatial autocorrelation in total tick number estimated by Moran's I (Sokal and Oden, 1978). Data are from the first visit in the colony and include nests of both treatments. Ten distance classes representing 10 m between marked nests have been defined. No index value was significantly different from zero. The same results were obtained using female count data only (results not shown).

Fig. 5

Spatial autocorrelation in the total tick number of counted nests, measured as Moran's I, across three distance classes: a, 1st visit; b, 2nd visit; c, 3rd visit; d, 4th visit; e, 5th visit; f, 6th visit. Circles indicate the autocorrelation coefficients. The same results were obtained with female count numbers.