Differences in the Vulnerability of Waterbird Species to Botulism Outbreaks in Mediterranean Wetlands: an Assessment of Ecological and Physiological Factors

Abstract

Avian botulism kills thousands of waterbirds every year, including endangered species, but information about the differences between species in vulnerability to botulism outbreaks and the capacity to act as carriers of Clostridium botulinum is still poorly known. Here, we estimated the vulnerability to botulism of 11 waterbird species from Mediterranean wetlands by comparing the number of affected birds with the census of individuals at risk. The capacity of different species to act as carriers was studied by detecting the presence of the C. botulinum type C/D botulinum neurotoxin (BoNT) gene in fecal samples and prey items of waterbirds in the wild and by the serial sampling of cloacal swabs of birds affected by botulism. We found differences among species in their vulnerabilities to botulism, probably related to feeding habits, season of arrival, turnover, and, possibly, phylogenetic resilience. The globally endangered white-headed duck (Oxyura leucocephala) showed mortality rates in the studied outbreaks of 7% and 17% of the maximum census, which highlights botulism as a risk factor for the conservation of the species. Invasive water snails, such as Physa acuta, may be important drivers in botulism epidemiology, because 30% of samples tested positive for the BoNT gene during outbreaks. Finally, our results show that birds may excrete the pathogen for up to 7 days, and some individuals can do it for longer periods. Rails and ducks excreted C. botulinum more often and for longer times than gulls, which could be related to their digestive physiology (i.e., cecum development). IMPORTANCEBotulism is an important cause of mortality in waterbirds, including some endangered species. The global climate change may have consequences in the ecology of wetlands that favor the occurrence of botulism outbreaks. Here, we offer some information to understand the ecology of this disease that can be useful to cope with these global changes in the future. We have found that some species (i.e., coots and dabbling ducks) are more vulnerable to botulism and have a more relevant role in the onset and amplification of the outbreaks than other species (i.e., flamingos and grebes). Feeding habits can explain these differences in part; in addition to the well-known role of necrophagous fly maggots, we found here that water snails are frequent carriers of Clostridium botulinum. This is relevant, because these water snails can thrive in eutrophic and polluted wetlands, exacerbating other changes driven by climate change in wetlands.A vian botulism is an intoxication characterized by a severe flaccid paralysis of the muscles and final death by respiratory failure caused by the botulinum neurotoxins (BoNTs) produced by different types of Clostridium botulinum (1). There are 7 types of BoNT single toxins, plus their mosaics (with characteristics of two toxins), and each one affects different animal species and/or humans. In particular, avian botulism outbreaks in freshwater waterbirds are generally caused by the mosaic type C/D (2, 3...

Development and Validation of a New Reliable Method for the Diagnosis of Avian Botulism

“…Ducks are known to be sensitive to botulism and to be one of the species the most affected by avian botulism [40, 41]. We also diagnosed two outbreaks involving swans.…”

Seasonal differences in drivers of species richness of waders in inland wetlands of La Mancha Húmeda Biosphere Reserve

“…Specifically, more than 2000 individuals from 19 species died between 1978 and 2008 (Vidal et al, ). For black‐winged stilt, occurring on many lakes in the study area, mortality rates of 1.8% and 85.3% were estimated in two botulism outbreaks in Navaseca Lake (MHBR region), with variation potentially caused by annual differences in turnover rates (Anza et al, ). An extended hydroperiod in summer can also attract other waterbird species (particularly moorhens, gulls and mallards), which may carry Clostridium botulinum (Anza et al, ; Vidal et al, ).…”

“…In wetlands receiving underground water, the hydroperiod contracts as a result of water extraction for agriculture overexploiting the aquifer (Florín & Montes, 1999 the risk of botulism outbreaks (Vidal et al, 2013), a key factor reducing waterbird populations throughout the world. In the MHBR region, botulism outbreaks have been recorded since 1978 (Vidal et al, 2013), affecting many wader species (Anza, Vidal, Feliu, Crespo, & Mateo, 2016;Minias, Włodarczyk, & Janiszewski, 2016). Specifically, more than 2000 individuals from 19 species died between 1978 and 2008 (Vidal et al, 2013).…”

Botulism in non-ruminants in Brazil

“…When birds ingest these larvae, they become intoxicated and develop botulism, commonly resulting in their death, and their subsequently becoming additional decomposing material for the potential development of larvae, closing the cycle (TAKEDA et al, 2006). This source of intoxication is extremely important, especially in countries with temperate climates where this cycle commonly culminates in seasonal outbreaks with extremely highmortality ratesin wildbirds (EVELSIZER et al, 2010;ANZA et al, 2016).…”

“…Although more common in aquatic birds, large botulism outbreaks can occur on commercial broiler farms, especially when there is a poor mortality removal, which leads to cannibalism of decomposing carcasses (SCHOCKEN-ITURRINO, et al, 1985;PIGATTO et al, 2007;SATO et al, 2016). There are several possible sources of intoxication by botulinum toxin for birds, including rotting food, drinking troughs containing fecal matter, and puddles and lagoons with stagnant water, especially during the dry season, when toxins become more concentrated in these water bodies (ALVES et al, 2013;LOBATO et al, 2013;ANZA et al, 2016). Fly larvae (maggots) present in cadavers and other decomposing materials constitute another important source of intoxication.…”