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Abstract - Blue-tongue of sheep is a viral disease that affects sheep clinically. The main vector, Culicoïdes imicola, is a tropical insect whose geographic distribution range was, until now, rarely reported north of the 40° line of North latitude. Its development is closely linked to climatic conditions. Over the last 2 years, the disease has spread to several countries in the Mediterranean basin, including France (Corsica). The forecasting models show that an increase in temperature would lead to an inevitable and lasting progression of the culicoïdes' population, which would put a large population of animals at risk from contamination.

BLue-tongue of sheep is a viral disease transmitted by insects which affects sheep clinically and can have serious economic implications due to loss of production, mortality and the regulatory restrictions which ensue.

The disease has increased in most Mediterranean countries over the last 2 years which raises a number of questions about the causes of the emergence particularly in the light of climate change. We need to ask ourselves whether the current epidemiology of blue-tongue in Europe could already be a sign of global warming and what impact climate change could have on the epidemiology of blue-tongue in Europe.

If we are to find any answers, without drawing any conclusions, it is important to look at the epidemiology of blue-tongue and a map of its evolution over the last 2 years before considering the outlook for the months and years to come.

Blue-tongue is a viral disease that affects wild and domestic ruminants. Sheep are the only domestic animals to show symptoms of the disease.

After an incubation period of 2-14 days, sheep show clinical signs of congestion and haemorrhaging. After a phase of prostration and intense hyperthermia, the animals show signs of congestion of the buccal mucous membranes with oedema of the tongue which can be cyanotic (hence the name "blue-tongue") and oedema of the lips and face. Then, there is discharge from the eyes and nose, podal lesions on the coronary pads and muscular stiffness. The disease may kill the animal spontaneously often because of the acute oedema of the lung or the animal may recover slowly but would no longer have an economic value.

Cattle and goats are also susceptible to infection. They multiply the virus but do not generally show any clinical signs. Therefore, they have an important role in the epidemiology of the disease.

In some countries like South Africa, wild ruminants act as a reserve for the disease. In Europe, red and fallow deer are susceptible and could play an important epidemiological role in zones where they are present in large numbers.

The virus in question is an orbivirus, of which there are known to be 24 different types in various parts of the world. It has been proven that immunity against one type of virus does not protect against a different type. Before vaccinating against blue-tongue, the types of virus in question must be properly identified. It is important to use as many strains of vaccine as there are viral strains present.

This virus is resistant but it is never found in the outside environment. It is not secreted in the various secretions that result from the disease. The disease is transmitted from one animal to another via the intermediary of a haematotrophic insect from the genus Culicoides.

Insects form the genus Culicoides are midges of 2-3 mm from the family Ceratopogonidae. A large number of species of Culicoides are blood-sucking but only some of them have a true vectorial capacity.

In Europe and Africa, only Culicoides imicola has been recognized as the main vector of the disease. Other vectors include C. variipennis in North America, C. insignis in South America, C. fulvus in Asia and C. brevitarsis in Australia.

Until now, the European species of Culicoides (C. obsoletus, C. newsteadi) have only been suspected of playing a role but their vectorial capacity has not yet been proven.

C. imicola is a tropical insect whose geographical distribution was only rarely reported north of the 40° line of North latitude until recently. Like most insects, the parameters that affect its population dynamics are closely linked to climatic conditions. Midges reproduce in conditions that are preferably humid and warm and where there is organic matter. The reproductive cycle takes about 3 weeks. C. imicola is often found near flocks.

After being infected with the virus, sheep and goats carry the disease in their blood for a maximum of 50 days before their immune system has developed sufficiently to get rid of it completely. This period is longer in cattle and can last up to 100 days. During this period new Culicoides can become infected.

The infection is spread geographically via the transport of Culicoides carriers or the movement of infected animals during the viraemic phase.

It has been reported that Culicoides can be carried by hot humid winds at low altitude (up to 1 500 m) across distances of up to 150 km.

We also know that C. imicola's power to infect is very temperature-dependent because the virus stops replicating in the insect when the temperature is below 15°C. In addition, the virus is not transmitted to the midges' progeny (no trans-ovarian transmission).

The activity of C. imicola is also very temperature-dependent. Its activity reaches a peak at around 24°C and it ceases to fly at temperatures below 18°C. Long cold periods kill adult C. imicola. However, it is capable of surviving short spells at temperatures slightly below zero.

Therefore, the survival of the infection in an infected zone is dependent on winter temperatures. Thus, in the early 1990s, Mellor modelled the zones that seemed to be the most favourable to the winter survival of C. imicola. In order to do this, he took a temperature indicator based on the monthly average of maximum daily temperatures of the coldest months. When this average is above +12.5°C, the zone is considered favourable to the survival of C. imicola.

On the map drawn by Mellor 10 years ago, we can see that Corsica (and even mainland France), is favourable to the survival of C. imicola (map 1).

A temperature rise of several degrees would mean that the zones favourable to the endemism of C. imicola would progress northwards and, therefore, could lead to a potential progression of the zones at risk from blue-tongue. Lastly, if for example C. imicola reached the French coast, it could temporarily spread across half of England during the hottest seasons.

Blue-tongue is present on all five continents. Given that its distribution is very dependent on vectors it is generally limited to the North between the 40th and 50th parallel and to the South between the 20th and 30th parallel.

These limits are obviously not very precise and they evolve as a function of climatic conditions or the intervention of temporary or seasonal vectors.

The countries in the Mediterranean basin are at the limit of the disease's distribution range. Since 1998, they have seen a considerable progression of the disease.

In 1998 and 1999, Greece reported the presence of three types of viral infection (4, 9 and 16) in the islands to the east of the country. In 1999, Bulgaria and Turkey experienced a epizootic disease with type 9 and type 4 respectively.

The infection due to the type 2 virus was first reported in Tunisia in January 2000 and then spread to Algeria in July of the same year. In August, Sardinia reported its first disease hot-spots followed by Sicily, Calabria, Corsica and the Balearic Islands in October.

Therefore, we are witnessing a real progression of the disease towards the north. Even though the zones recently affected are within the zones that have been known to be at risk for a long time, the novelty here is the danger of the infection becoming permanent because of the lasting establishment of C. imicola which seems to have found ecosystems favourable to its survival.

In Corsica, the disease seriously affected sheep production between October and December 2000. Forty-nine disease hot-spots containing 12 000 sheep were confirmed. Two-thirds of the hot-spots were identified in southern Corsica where mortality rate reached on average 41%.

The serological analyses conducted on cattle and sheep showed that the infection was widespread across the whole island (maps 2 and 3). However, the serological prevalence was twice as high in southern Corsica as in northern Corsica (table 1). This difference could mean that the disease arrived in the south in 2000 or that the conditions for vector multiplication are less good in the north of the island.

Table 1: Serological prevalence of blue-tongue in the Corsican flocks and herds

	Cattle			Sheep
	Herds tested	Animals tested	Positive	Flocks tested	Animals tested	Positive
Northem Corsica	31	1216	24%	18	2095	16%
Southem Corsica	23	1021	40%	21	2609	38%

C. imicola, which has never been reported in Corsica before, was captured on the island from the start of October along with other blood-sucking species that are encountered more traditionally at these latitudes (map 4). Since then, its presence has been confirmed all over the island apart from Cape Corse.

The disease has had a serious economic impact on the Corsican livestock sector. The direct losses were due to the high mortality rates in some production units and the large number of sick animals in production units in southern Corsica. This was because the animals had no immunity against the disease which was new to them. The regulatory measures were also expensive. These included compensation payments for the slaughter of sick animals and the implementation of a mass vaccination programme during the winter of 2000-2001.

Lastly, following the declaration of Corsica as an infected zone, trade restrictions were imposed banning the exports of all live animals to disease-free zones.

The future of blue-tongue in Corsica depends largely on the survival of the main vector. The climatic conditions during the winter of 2000-2001 were particularly favourable to C. imicola which is why there is a high risk that the disease will continue. In addition, the presence of cattle, which could act as a temporary domestic reserve, increases the risk of the spread of infection even though the sheep flock has been vaccinated.

The future also looks gloomy because of the risk of the appearance of new serotypes of virus, such as type 9 which has already been reported in Calabria.

By extension, the survival of the infection in Corsica puts continental France in direct danger of an introduction of the infection. The Alpes Maritimes and Var coasts are, in fact, only 180 km from the Corsican coast and the possibility of a favourable wind carrying infected Culicoides cannot be ruled out. Other modes of transport (cars, boats) could also play a role in carrying C. imicola. In order for an infection to develop, C. imicola has to find conditions that are favourable to its development which again depend on climatic conditions.

At this stage we do not have enough information to be able to answer the first question which is raised by the recent evolution of blue-tongue, in other words the part played by climatic change in the epidemiological picture.

Evidently, we are witnessing a progression of infected regions towards the north, but Corsica has always been part of the zones potentially at risk from the disease. However, this is the first time that C. imicola has been found in Corsica and in large numbers as well. The first insects captured in 2001 confirm the presence of C. imicola as far as the north of the island which indicates that the vector is well established in Corsica.

We have also observed a serological prevalence gradient on the island which goes from the south to the north. This could potentially be linked to the density gradient of C. imicola.

However, we cannot be certain about the previous history of C. imicola in Corsica because the last entomological prospecting for Ceratopogonidae was several decades ago.

We could also question the effects that climate change could have on the evolution of blue-tongue.

Based on Mellor's model which forecasts that a temperature rise of 1°C would mean that C. imicola populations would move north by 90 km, it seems very likely that global warming would lead to the vector spreading to the Spanish, French and Italian coasts and the disease would probably spread in the same zones.

This spread would encourage epizootic outbreaks of the disease further north on the French mainland which would favour the seasonal multiplication of vectors.

The arrival of blue-tongue on the continent would have very significant consequences in terms of trade restrictions. In fact, the EU recommends a protection and surveillance zone of 150 km around the confirmed disease hot-spots. The difficulty involved in defining the precise limits of these zones would be added to the difficulties of animal trading throughout the Mediterranean zone.

Apart from vaccinating in the infected zones, the priority for action is to concentrate on epidemiological monitoring both in the infected and the disease-free zones.

In infected regions, the purpose of the surveillance is to evaluate the efficacy of the control measures that have been implemented, to monitor the appearance of new viral types and to study the vectors' population dynamics. In disease-free regions, the purpose of surveillance is to verify the absence of the disease (clinical surveillance and screening) and of the main vector of the disease.

A large number of stakeholders are involved in this surveillance. First and foremost is the Ministry of Agriculture (the central administrative body for food) and its decentralized services, CIRAD and AFSSA for serological and virological surveillance, EID Méditerranée and the Louis Pasteur University of Strasbourg for entomological surveillance.

Blue-tongue is undoubtedly progressing northwards. Even though we cannot clearly confirm that this progression is a result of global warming, the trends we have observed would suggest that this is the case. As a result, an increase in temperature would most probably be reflected in the continued spread of the distribution range of the vectors and the disease towards the north with considerable economic implications.

Blue-tongue is just one example of the risks for animal health that could be induced by climatic change. It is a good example of the spread of a vectorial disease. Other diseases, such as African horse fever can be transmitted by the same vector and other vectorial species could see their distribution range evolve as a function of climate change.

In the face of these new emerging risks, there is a lot to gain by pooling the expertise of all the partners involved in risk analysis and surveillance in the form of an observatory in the south for the surveillance and warning of emerging diseases.

Map 1. Modeling of the zones favourable to C. imicola, according to P. Mellor

Map 2. Serology in cattle production units from October to December 2000	Map 3. Serology in sheep production units from October to December 2000
Map 4