Predicting West Nile Virus Seroprevalence in Wild Birds in Senegal

Abstract

West Nile fever epidemiology is complex, and the role of birds in the maintenance, amplification, and dissemination of the West Nile virus (WNV) remains partially unknown. In 2003, a serological study was performed in Senegal, where West Nile infection is considered endemic. The goal was to identify potential reservoirs of WNV among bird species present in the Ferlo area (northern Senegal) and the Senegal River Valley, and to screen the ecological factors possibly related to West Nile infection. Serological data were analyzed using a generalized linear model. Statistical association between ecological factors and the risk of infection were then modeled to derive a species-specific risk. A cross-validation was conducted. The overall observed prevalence rate was 5.5% (n = 422). Thirteen bird species were found positive, from which five were migrating: Lanius senator, Anthus trivialis, Hippolais opaca, Jynx torquilla, and Cercotrichas galactotes. The nesting type in resident birds was positively correlated with the risk of infection (odds ratio [OR] = 11, p = 0.0003); the gregariousness level of birds appeared as a protective factor (OR = 0.3, p = 0.01). The predicted prevalence varied between 1% and 39% for resident species and between 1% and 7% for migrating species. Results of model internal validation were satisfactory at the individual and species level. However, more field and experimental investigations are needed to confirm these preliminary results and help target the future research and surveillance in Senegal.

Introduction

W est Nile fever is an emerging arbovirosis caused by the West Nile virus (WNV) (Flavivirus, Flaviviridae). The epidemiological cycle involves wild birds and Culicidae mosquitoes (mainly Culex genus). Horse and man are dead-end hosts but the disease is a veterinary and human public-health issue. The role of birds in the maintenance, amplification, and dissemination of the virus remains partially unknown. Recent studies suggested that the bird community structure, diversity, and presence of particular species may determine the mosquito infection rate (Kilpatrick et al. 2006). Nestling as well as hatch-year birds may be important factors of amplification (Scott and Edman 1991, Hamer et al. 2008).

In Senegal, the WNV was isolated several times from Aedes and Culex mosquitoes in the Senegal River Valley (Traore-Lamizana et al. 1994). Different serological surveys, undertaken in the Ferlo area (northern Senegal) in humans (Murgue et al. 2002), horses (Chevalier et al. 2006), and sentinel chickens (Chevalier et al. 2007), suggested that the WNV transmission regularly and intensively occurred in this country.

In Senegal, the avian biodiversity is high, especially in the Senegal River Valley, which is a major wintering area for European migratory birds.

To target future research and surveillance, we sought to identify ecological factors linked to the risk of West Nile infection. A serological survey was conducted to estimate the serological point prevalence of anti-WNV antibodies in resident and local or Palearctic migratory bird species. Statistical association between ecological factors and the risk of infection was then evaluated and modeled to derive a species-specific risk.

Material and Methods

Study areas

Two study sites were selected based on previous studies (serology) and expert knowledge (ornithology). The first site was in the close vicinity of the Barkedji village, in the Ferlo area (Fig. 1). The Ferlo is a Sahelian region characterized by temporary ponds that fill up in July and remain flooded until November–December. When flooded, ponds constitute a favorable biotope for Aedes and Culex mosquitoes. Many species of endemic birds nest around these ponds, and migratory birds are attracted by the water and abundant food (Morel and Morel 1978).

FIG. 1.

Location of the Barkedji village and the Djoud'j National Park (PNOD) in Senegal.

The second site was located in the Djoud'j National Park (PNOD; Fig. 1). The PNOD is a large wetland located in the Senegal River delta, made of a large lake surrounded by streams, ponds, and backwaters.

Bird trapping

Birds nesting in Barkedji leave in December when ponds dry up. Birds were trapped from September 28 to October 7, 2003 in Barkedji to guarantee the trapping of both resident and migrating birds. The trapping period was similar in the PNOD. Ground-level mist nets (12 × 2.8 m, 36-mm mesh) were used to focus on passerine birds, which are supposed to play a prominent role in the epidemiological cycle of WNV (Komar et al. 2003). Nets were operated from sunrise to 11 A.M. and from 5 p.m. to sunset. Birds were sampled from the wing or jugular vein. Sera were centrifuged and stored at 4°C until they were transported to Dakar.

Serological analysis

Sera were analyzed using an epitope-blocking enzyme-linked immunosorbent assay using the antigen used by Blitvich et al. (2003).

This test was performed using the WNV-specific monoclonal antibody (MAb) 3.1112G (Chemicon, Rosemount, IL). The original technique was slightly modified: WNV antigen (100 μL, 1/4000 in 50 mM NaHCO₃, 50 mM Na₂CO₃, pH 9.6) was coated overnight at 4°C, followed by 1 hour at 37°C, on Maxisorp 96-well plates (NUNC, Thermo Fisher Scientific, Roskilde, Denmark). Plates were washed four times with phosphate-buffered saline (PBS; pH 7.4) containing 0.1% Tween 20, blocked with 200 μL of blocking buffer (PBS containing 0.1% Tween 20 and 0.2% bovine serum albumin) at 37°C for 45 minutes, and washed again. Fifty microliters of sera diluted 1/10 in blocking buffer were added to each well, and incubated at 37°C for 2 hours. After four washes, 50 μL of MAb, diluted 1/4000 in blocking buffer, was added to each well and incubated for 1 hour at 37°C, followed by 1 hour at 4°C. After four more washes, 50 μL of horseradish peroxidase labeled rabbit anti mouse immunoglobulin G (Serotec; Oxford, UK), diluted 1/500 in blocking buffer, was added to each well and incubated for 1 hour at 37°C. After four washes, 200 μL of tetramethylbenzidine substrate (Sigma Aldrich, St. Louis, MO) were added. After 30 minutes, optical densities were measured at 630 nm. The ability of the test sera to block the binding of the MAbs to WNV antigen was compared to the blocking ability of chicken serum without antibody to WNV (Vector Laboratories, Burlingame, CA). Data were expressed as relative percentages. An inhibition value ≥ 30% was considered to indicate the presence of viral antibodies.

Data analysis

Seven factors possibly related with the exposition of birds to mosquito bites were included as explanatory variables: the trapping location (Barkedji, PNOD), the migratory status (resident in Africa, or migratory breeding outside Africa), the feeding behavior (flying or settled), the resting site (ground, bush, canopy), the type of nest (on the ground, platform, cup or cavity nest—so-called “medium, or bulky” nest), the herd instinct level (high, low), and the affinity with urban areas (high, moderate, low). Among these variables, the nest type was treated specifically because of its particular meaning: as the exposure level of birds during the breeding season depends on nesting location, the nest type effect cannot be dissociated from the nesting site effect (i.e., the migrating status). Therefore in the analysis, the nesting type variable was studied separately in resident and in migratory birds.

A bivariate analysis using Fisher exact test was performed to assess the relation between the observed prevalence rate and each variable. Variables associated with serological point prevalence (p value ≤ 0.20) were selected for inclusion in a logistic regression model where the individual serological status (positive or negative serum) was the response variable. For the reasons detailed above, the nest type variable was not included alone but only in interaction with the migrating status variable. A stepwise procedure was performed to select the best model according to the Akaike information criterion (Burnham and Anderson 2002). Odds ratios (ORs) and their confidence intervals (CIs) were computed for the explanatory variables of the resulting model, and the model was used to predict the prevalence rate and its CI for each combination of ecological characteristics corresponding to the tested species.

A cross-validation was conducted (Stone 1974): half of the tested birds were randomly chosen for fitting the model, which was then used to predict the serological status of the remaining birds. Prediction error was evaluated at the individual level and at the species level. Individual-level error was the usual proportion of incorrect predictions. For species-level cross-validation, two prevalence classes were considered to distinguish low prevalence species (<10%) and high prevalence species (>10%). Prediction error was the proportion of misclassified species, weighted by the number of tested animals.

Results

Serological results

A total of 422 birds were sampled, belonging to 16 families and 49 species. One hundred seventy birds were trapped in Barkedji, belonging to 8 families and 16 species, most of them being resident (89%). In the PNOD, 252 birds were sampled, belonging to 13 families and 33 species. Most of them were migratory (80%). The most frequently trapped birds belonged to the Muscicapidae family (29%, n = 122), followed by the Ploceidae (24%, n = 100), the Columbidae (12%, n = 51), and the Alcedinidae (8%, n = 35).

The overall observed prevalence rate was 5.5% (n = 422). Anti-WNV antibodies were detected in 23 birds from 7 families and 13 species, among which five were migrating: Woodchat Shrike (Lanius senator), Tree Pipit (Anthus trivialis), Western Olivaceus Warbler (Hippolais opaca), Eurasian Wryneck (Jynx torquilla), and Rufous Scrub-robin (Cercotrichas galactotes).

For 19 species, the number of trapped birds was ≥5, representing 87% of the totality of tested birds (n = 369). Among these species, the prevalence rate was >10% for each of the three Columbidae species, as well as in two Muscicapidae species. The prevalence rate was <10% for H. opaca and Ploceus cucullarus. No positive bird was found for the 13 other species with ≥5 trapped birds (Table 1).

Table 1.

Ecological Characteristics and Observed Serological Prevalence of West Nile Fever in 19 Bird Species of Which ≥5 Individuals Were Tested in Two Different Areas (Ferlo, Senegal River Basin) of Senegal in 2003

Family	Species	Migrating status ^a	Nest type ^b	Resting site ^c	Herd instinct ^d	Feeding behavior ^e	Urban affinity ^f	Observed prevalence	Predicted prevalence (%)	95% CI ^g
Alcedinidae	Alcedo cristata	R	G	B	L	F	L	0/17	<6	0–0.03
	Halcyon senegalensis	R	M	C	L	F	L	0/15	<7	0.006–0.14
Charadriidae	Calidris minuta	M	G	G	H	S	L	0/9	<1	0–0.03
	Actitis hypoleucos	M	G	G	H	S	L	0/13	<1	0–0.03
Columbidae	Oena capensis	R	M	G	H	S	M	2/9	15	0.068–0.24
	Streptopelia senegalensis	R	M	C	H	S	H	2/8	15	0.068–0.24
	Streptopelia vinacea	R	M	B	H	S	M	4/31	15	0.068–0.24
Hirundinidae	Riparia riparia	M	G	C	H	F	L	0/13	<1	0–0.03
Meropidae	Merops persicus	M	G	C	H	F	L	0/21	<1	0–0.03
Motacillidae	Motacilla alba	M	M	G	L	S	M	0/6	<7	0.006–0.14
	Motacilla flava	M	G	G	H	S	L	0/18	<1	0–0.03
Muscicapidae	Hippolais opaca	M	M	B	H	F	L	1/17	2	0–0.04
	Phylloscopus trochilus	M	M	B	H	F	L	0/45	<2	0–0.04
	Sylvia cantillans	M	M	B	H	F	M	0/29	<2	0–0.04
	Cercotrichas galactotes	M	M	B	L	S	L	1/6	7	0.006–0.14
	Cercotrichas podobe	R	M	B	L	S	M	4/9	39	0.17–0.61
	Phoenicurus phoenicurus	M	M	B	L	S	M	0/5	<7	0.006–0.14
Ploceidae	Ploceus cucullatus	R	B	C	H	S	H	2/53	2	0–0.04
	Ploceus melanocephalus	R	B	C	H	S	H	0/45	2	0–0.04

Prevalence is predicted for the corresponding combinations of herd instinct, nest type and migration status; confidence intervals (CIs) refer to these combinations.

R, resident in Senegal; M, migratory, breeding outside Senegal.

B, bulky nest; M, medium (platform, cup or cavity) nest, G, nest built on the ground.

G, ground; B, bush; C, canopy.

L, low; H, high.

S, settled; F, flying.

L, low; M, moderate; H, high.

CI of the predicted prevalence.

The 13 remaining species were weakly represented, with <5 trapped animals per species. Positive birds were found in six of these species (Table 2): both tested Laniidae species, Urocolius macrourus (Coliidae), Jynx torquilla (Picidae), Ploceus velatus (Ploceidae), and Anthus trivialis (Motacillidae).

Table 2.

Ecological Characteristics and Observed Serological Prevalence of West Nile Fever in 30 Bird Species of Which <5 Individuals Were Tested in Two Different Areas (Ferlo, Senegal River Basin) of Senegal in 2003

Family	Species	Migrating status ^a	Nest type ^b	Resting site ^c	Herd instinct ^d	Feeding behavior ^e	Urban affinity ^f	Observed prevalence	Predicted prevalence (%)	95% CI ^g
Alaudidae	Galerida cristata	R	G	G	L	S	M	0/1	<6	0–0.12
Alcedinidae	Halcyon leucocephala	M	G	C	L	F	L	0/3	<4	0–0.12
Bucerotidae	Tockus erythrorhynchus	R	M	C	H	S	L	0/1	<15	0.068–0.24
Caprimulgidae	Caprimulgus climacurus	R	G	G	L	F	L	0/2	<6	0–0.12
Charadriidae	Calidris alpina	M	G	G	H	S	L	0/1	<1	0–0.03
	Charadrius hiaticula	M	G	G	H	S	L	0/1	<1	0–0.03
	Rostratula bengalensis	R	G	G	L	S	L	0/1	<6	0–0.12
	Tringa ochropus	M	M	G	L	S	L	0/1	<7	0.006–0.14
	Vanellus spinosus	R	G	G	H	S	L	0/2	<1	0–0.04
Coliidae	Urocolius macrourus	R	M	C	H	F	L	1/3	15	0.068–0.24
Columbidae	Columba guinea	R	M	C	H	S	H	0/2	<15	0.068–0.24
	Turtur abyssinicus	R	M	B	H	S	M	0/1	<15	0.068–0.24
Coraciidae	Coracias abyssinicus	R	M	C	H	F	L	0/1	<15	0.068–0.24
Laniidae	Laniarius barbarus	R	M	B	L	S	M	1/1	39	0.17–0.61
	Lanius senator	M	M	B	L	S	L	1/3	7	0.006–0.14
Laridae	Larus cirrocephalus	R	G	G	H	S	M	0/1	<2	0–0.04
Meropidae	Merops pusillus	R	G	C	H	F	M	0/4	<1	0–0.04
Motacillidae	Anthus trivialis	M	G	G	H	S	L	1/2	1	0–0.03
Muscicapidae	Terpsiphone viridis	R	M	C	H	F	L	0/1	<15	0.068–0.24
	Camaroptera brachyura	R	B	B	L	S	M	0/2	<6	0–0.12
	Hippolais polyglotta	M	M	B	H	S	L	0/2	<2	0–0.04
	Sylvia atricapilla	M	M	B	H	S	M	0/4	<2	0–0.04
	Sylvia borin	M	M	B	H	S	M	0/1	<2	0–0.04
	Sylvia hortensis	M	M	B	L	S	M	0/1	<7	0.006–0.14
Picidae	Jynx torquilla	M	M	B	L	S	L	2/3	7	0.006–0.14
	Mesopicos goertae	R	M	C	L	F	L	0/2	<39	0.17–0.61
Ploceidae	Ploceus luteolus	R	B	B	H	S	M	0/1	<2	0–0.04
	Ploceus velatus	R	B	B	H	S	M	1/1	2	0–0.04
Sturnidae	Lamprotornis caudatus	R	M	C	H	S	M	0/1	<15	0.068–0.24
	Lamprotornis pulcher	R	M	G	H	S	M	0/3	<15	0.068–0.24

Prevalence is predicted for the corresponding combinations of herd instinct, nest type and migration status; confidence intervals (CIs) refer to these combinations.

R, resident in Senegal; M, migratory, breeding outside Senegal.

B, bulky nest; M, medium (platform, cup or cavity) nest, G, nest built on the ground.

G, ground; B, bush; C, canopy.

L, low; H, high.

S, settled; F, flying.

L, low; M, moderate; H, high.

CI of the predicted prevalence.

Bivariate analysis

Prevalence rate was higher in resident (8.4%, n = 203) than in migrating birds (2.7%, n = 219; p = 0.02), whereas these rates were similar for birds trapped in the PNOD (4.8%, n = 252) and in Barkedji (6.5%, n = 170; p = 0.51).

The prevalence rate was higher in species showing a low herd instinct (11.5%, n = 78) than in gregarious species (4.1%, n = 344; p = 0.02).

In resident birds, a high prevalence rate was observed in species building medium nests (19.2%, n = 73), whereas low rates were observed for the two other types: 2.9% for birds building bulky nests (n = 102) and 0.0% for birds nesting on the ground (n = 28; p ≤ 0.0001). In migratory birds, nesting type was not associated with prevalence rate; none of the migratory birds belonged to species building bulky nests; prevalence rate was similar for the two other nesting types: medium nests (3.6%, n = 138) and nests built on the ground (1.2%, n = 81; p = 0.41).

Birds feeding on flight were as frequently infected (4.8%, n = 167) as birds feeding settled, in trees, or on the ground (5.9%, n = 255; p = 0.67). Prevalence rate was high in birds resting on the ground (10.2%, n = 88), with lower values being observed in birds resting in bush (4%, n = 125) or in the canopy (4.3%, n = 209; p = 0.11). Last, affinity with urban areas was not associated with the prevalence rate, ranging from 3.7% (n = 107) for birds living in villages, 8% (n = 160) for peridomestic birds, and 3.9% (n = 154) for birds living far from urban areas (p = 0.25).

Logistic model

The explanatory variables selected for inclusion in the logistic regression model were: the migration status, the herd instinct, the resting site, and the interaction between the migration status and the nest type. As none of the migratory birds belonged to a species building bulky nests and as similar prevalence rates had been observed in species building bulky nests and in species nesting on the ground, the nest type variable was recoded in two categories: medium nests and other nest types (bulky nests and nests built on the ground). The stepwise model selection procedure led to the exclusion of the resting site variable, and the resulting model thus included the migration status and its interaction with the nest type, and the herd instinct (Table 3). The largest effect was attributed to the nest type in resident birds with an OR of 11.0 (p = 0.0003) for medium nests (reference: bulky nests or nests built on soil), whereas the nesting type effect was not significant in migratory birds. High herd instinct (reference: low) had a protective effect with OR of 0.3 (p = 0.01).

Table 3.

Results of the Logistic Model Selected by the Stepwise Regression Procedure

Variable	Reference	Value	OR (95% CI)	p value ^a
Migration status	Migrating	Resident	1.4 (0.2–29.6)	0.8
Nest type: migrating birds	Bulky or soil nest	Medium nest	1.9 (0.3–37.9)	0.6
Nest type: resident birds	Bulky or soil nest	Medium nest	11.0 (3.6–49.8)	0.0003
Herd instinct	Low	High	0.3 (0.1–08)	0.01
Intercept			0.006 (0.0003–0.03)	<0.0001

OR, odds ratio; CI, confidence interval.

Wald test.

Predicted prevalence varied between 1% and 39% for resident species and between 1% and 7% for migratory species. This predicted prevalence (and its CI) refers to combinations of ecological characteristics (herd instinct and interaction between nest type and migration status); therefore, species sharing the same ecological characteristics have identical predicted prevalence and CIs (Tables 1 and 2). Cross-validation procedure yielded an individual prediction error of 5%: when half of the data set was left out when fitting the model, predicted serological status for the other half was correctly predicted for 95% of the birds. At the species level, prediction error was 11%: 89% of the species were correctly classified either as low prevalence (<10%) species or as high prevalence (>10%) species.

When considering the 19 species for which ≥5 birds were trapped (Table 1), the predicted status (low versus high prevalence) was correct in all species. High prevalence status was predicted (and observed) for four resident species and none of the migratory species. Low prevalence status was predicted for 11 migratory species and four resident species.

Model predictions were correct for two-thirds of the 30 weakly represented species (<5 tested birds; Table 2). A high-prevalence status was predicted for 10 resident species, among which, Urocolius macrourus and Laniarius barbarus were found positive with prevalence figures of 1/3 and 1/1, respectively. Conversely, the model predicted a low prevalence level for nine resident species and for 11 migratory species, positive results being observed in one resident species (Ploceus velatus: 1/1) and in three migratory species (Anthus trivialis: 1/2, Lanius senator: 1/3, and Jynx torquilla: 2/3).

Discussion

The overall serological prevalence rate (5.5%) confirmed that WNV was transmitted to wild birds in Senegal either in the Ferlo or in the Senegal River basin. Senegal, where the WNV circulation is endemic, is also a major area of wintering for Palearctic migrating birds. To explain the WNV presence in Palearctic areas, current epidemiological knowledge assumes that the virus may be regularly transported from Africa to Europe by migrating birds (Malkinson and Banet 2002). The higher prevalence rate observed in our study in resident birds (8.4%)—compared with migratory species (3%)—is consistent with this assumption: the exposure to the virus was longer in the former than in the latter species.

In migratory birds, the prevalence rate of 2.7% was close to observations made in birds sampled in southern France in 2004 possibly coming from sub-Saharan Africa (Jourdain 2006). Birds' serological status is not related to their epidemiological role in WNV transmission. A large number of birds should be ringed in Senegal and trapped and tested for viral presence when arriving in Europe to accurately assess the risk of introduction of the virus in Europe by these birds.

Large variations of the observed point prevalence are reported in the literature. In the West Indies in 2002, it ranged from 3.3% in Jamaica (n = 542; Dupuis et al. 2003) to 15% (n = 33) in Dominican Republic (Komar et al. 2003). In the African continent, point serological prevalence rates was 40% in the Nile delta, Egypt, in 1950 (n = 420; Taylor et al. 1956) and 12.5% in South Africa in 1962–1965 (Jupp 2001). In the Middle East, seroprevalence rate was 11.5% and 11.3% on resident birds in Israel in 1965–1966 (Nir et al. 1969, 1972). However, comparisons are difficult because the ecosystems and epidemiological situations differ. Within the same area, large differences were also observed between species: in Egypt, the point prevalence was 13% in domestic chicken (n = 15) and 65% in hooded crows (n = 163; Taylor et al. 1956). However, our results corroborate some results of previous studies: the high point prevalence observed in the Columbidae family was reported in Israel (Nir et al. 1969, 1972); Woodchat Strike (Lanius senator) was identified as candidate species for virus introduction from sub-Saharan Africa to Europe (Jourdain 2006).

More information is needed on the biology of the sampled species. As a matter of fact, seroprevalence is an indirect indicator of the exposure since other factors may influence its value. The high prevalence rate in Streptopelia species may be explained by the fact that they live in, or close to, urban areas, which are preferential habitats for Culex mosquitoes, but also by a greater longevity compared with birds of other families. Bird age may be a confounding factor to study the exposure level using serological data. Juvenile and adult birds can be easily distinguished. However, this distinction is not accurate enough to take into account the age as a confounding factor. Due to a lack of field method to precisely estimate bird ages, this factor could not be considered in this study.

The most important risk factor observed in this study was the interaction between migration status and nest type. As previously suggested, nesting could be a predominant period for WNV infection: the limited mobility of adults and fledglings, and the bare skin of the latter, presumably make them easy prey for mosquitoes (Marra et al. 2004). The nesting type would then be an important factor to explain bird exposure to mosquito bites. In resident birds, high prevalence was associated with medium nests that include platform, cupped, and cavity nest. Platform nests are rudimentary, flat structures located on the ground, in a tree, or on the tops of rooted vegetation or debris in shallow water. Cupped nests are an arrangement of hard and soft material from floor and walls shaped in a cup. Cavity nest is a hollowed-up opening in the trunk of a tree. These three kinds of nests are located in the midstory and provide a large access to mosquitoes. Ground nests are usually just scrapes on the ground forming a depression. Many mosquito' species exhibit vertical height specialization for host seeking (Balenghien et al. 2006): birds building nests on the ground may be less exposed than birds building medium nests. The structure of bulky nests is complex and compact. They are made of twigs or grass weave or not with a grass-lined chamber inside. Access to outside is rather reduced; thus, the exposure to mosquito bites of birds building these kinds of nest is probably weak.

The increased point prevalence in nongregarious birds might be explained by a dilution effect previously suggested in horses (Durand et al. 2002).

Results of model internal validation were satisfactory at the individual and species level. Considering two prevalence classes (below or above 10%), the model adequately fitted the status of each species with ≥5 trapped birds, thus giving some confidence in model predictions. However, an external validation remains to be performed using independent data. The higher predicted prevalence in migratory birds was 7%, in particular for White Wagtail (Motacilla alba), the Common Redstart (Phoenicurus phoenicurus), and the Rufous Scrub-Robin (Cercotrichas galactotes). Previous studies in 1965–1967 in Israel suggested that the White Wagtail was exposed to the WNV and might be a relevant indicator of WNV circulation for surveillance (Nir et al. 1969, 1972). The Common Redstart was reported as having WNV antibodies in another study in southern France in 2004 (Jourdain 2006). To our knowledge, no infection of Rufous Scrub-Robin by WNV was reported in the literature. However, our analysis provides evidence that these migratory species are possibly exposed to WNV and might play a role in the dissemination of WNV from Africa to Europe. Finally, high prevalence rates were predicted for three resident species: the Black Shrub-Robin (Cercotrichas podobe), the Common Gonolek (Laniarius barbarus), and a woodpecker species (Mesopicos goertae). Nothing is known about the susceptibility to the WNV and the reservoir competence of these two species. More field and biological data are needed to confirm these preliminary results.

Footnotes

Acknowledgments

This publication is catalogued by the EDEN Steering Committee as EDEN00116 (www.edenfp6project.net). The contents of this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission.

Disclosure Statement

This publication was partially funded by the CORUS project (French Ministry of Foreign Affairs) and GOCE-2003-010284 EDEN grants.

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