Waterfowl—The Missing Link in Epidemic and Pandemic Cholera Dissemination?

Cholera, a life-threatening diarrhoeal disease, has afflicted human beings and shaped human history for over two millennia. The disease still kills thousands of people annually. Vibrio cholerae, the etiologic agent of cholera, is endemic to aquatic environments [1], but despite intensive research efforts its ecology remains an enigma. The fatal effects of cholera are mainly due to the toxin produced by specific serogroups (O1 and O139) of V. cholerae [1]. Strains of V. cholerae that belong to serogroups other than O1 and O139, collectively referred to as the non-O1, non-O139 V. cholerae, have also been implicated as etiologic agents of moderate to severe human gastroenteritis [2]. The disease is endemic in Southern Asia and in parts of Africa and Latin America, where outbreaks occur widely and are closely associated with poverty and poor sanitation. The epidemic strains spread across countries and continents over time, giving rise to cholera pandemics [1]. It has been suggested that zooplankton function as a carrier of V. cholerae via ocean currents. However, the mechanism that enables V. cholerae to cross freshwater bodies within a continent, as well as oceans between continents, remains unknown. Here, we put forward a strongly neglected hypothesis that deserves more attention, and discuss evidence from the scientific literature that supports this notion: migratory water birds are possible disseminators of V. cholerae within and between continents. V. cholerae has been associated with crustaceans and especially copepods [1,3,4]. Copepod eggs hatch into nauplius larvae. The life cycle typically includes six naupliar stages and six copepodite stages, the last of which is the adult stage. These small crustaceans are found almost everywhere that water is available. Chironomids (Chironomidae, Diptera), also known as non-biting midges, are closely related to mosquitoes (Culicidae), but female chironomids do not bite or feed. They undergo complete metamorphosis of four life stages: eggs, larvae, pupae (aquatic stages), and adults that emerge into the air. Chironomids have also been found to serve as intermediate host reservoirs and possible windborne carriers for V. cholerae [5–7]. Although adult chironomids can fly and carry V. cholerae [8], they disperse over short distances of less than 1 km [9]. Dispersal of the adults by wind [8,10] is restricted in its orientation and unlikely to be directed towards suitable habitats. Thus, chironomid movement by wind is probably not responsible for the long-distance dispersal of V. cholerae (Figure 1, course III). Chironomids and copepods are abundant in aquatic ecosystems and are a major dietary component of many residential and migratory waterfowl [11]. Recently, reported evidence has suggested that larvae of Chironomus salinarius and Copepoda can survive the gut passage (endozoochory) in several bird species [12,13]. The chironomid larvae were found to survive gut passage in the black-tailed Godwits (Limosa limosa) on autumn migration in southwest Spain [12]. Godwits and other waders move regularly over distances of up to 20 km between feeding and roosting sites while resting at stopover sites [14], thus facilitating passive dispersal between different water bodies within a wetland complex. Godwits fly at speeds of 60 km per hour [15], and could potentially disperse chironomid larvae over great distances during their migration between breeding areas in northern Europe and wintering areas in Africa [16] (Figure 1, course I). Recent evidence indicates that viable copepods and chironomids are externally attached to birds’ feet and feathers (epizoochory) [13]. Thus, endozoochorous and epizoochorous dispersal of these invertebrates via waterfowl may be a common phenomena and important process for V. cholerae dissemination (Figure 1, course I). We recently isolated and identified V. cholerae non-O1 from the gut of several individual fish (Tilapia sp.) from various freshwater bodies in northern Israel (unpublished data). Tilapia is known to consume copepods and chironomids [17], and hence we assume that these food items, as well as other invertebrates, might well be the source of V. cholerae in the fish gut. Thus, we suggest that fish also function as intermediate reservoirs of V. cholerae (Figure 1, course II). Support for the finding that V. cholerae survive in fish comes from the fact that some cholera outbreaks have been correlated with the consumption of uncooked fish. Cholera was associated with the eating of salt fish, sardines, and other fish from an atoll lagoon [18]. Consumption of dried fish was significantly correlated with risk of cholera in Tanzania [19]. Three cases of cholera in Sydney, Australia, were reported in 2006. A food trace-back investigation revealed that the only factor common to all cases was the consumption of raw whitebait imported from Indonesia [20]. V. cholerae was isolated from fish called ‘‘lorna’’ (Sciaena deliciosa) that were caught in inshore waters in Peru during a Peruvian epidemic [21]. It was postulated that cholera endemicity in India was due to hilsa fish [22]. Moreover, seafoods, including mollusks, crustaceans, crabs, and oysters also feed on plankton and can become infected with V. cholerae [3,4,23].