Avian Botulism Die-Offs: The Mystery Continues

Waterfowl spring migration in the United States. Avian botulism outbreaks can kill millions of birds in a single season. USFWS

Waterfowl spring migration in the United States. Avian botulism outbreaks can kill millions of birds in a single season.     USFWS

Late summer and fall are prime time for die-offs of ducks, geese, and other wild water birds due to the toxin that causes botulism. This year is no different in the northern hemisphere, with small outbreaks reported in Colorado and North Carolina in the United States, and France and possibly the UK in Europe.

Since waterfowl die-offs due to botulism were first reported little more than a century ago in western North America, the disease has spread to over 28 countries today, many only since the 1970s.  Periodic outbreaks leave hundreds of thousands to millions of birds dead.

Avian botulism appeared and accelerated in lockstep with the exponential growth in the human population, and in particular the latter’s altering of wetland ecosystems. But just how to explain this association is not easy. Unprecedented environmental changes over the past two decades have witnessed not an increase in, but rather an absence of mass avian botulism die-offs. While our understanding has improved, we are nevertheless little closer to predicting and controlling these outbreaks today than we were a century ago.

Strange mass waterfowl die-offs were first noticed in the 1890s in California, and again between 1909-13, when millions of birds died on Utah’s Great Salt Lake, in California’s San Joaquin valley wetlands, and on the prairies of Saskatchewan, Canada.

Initially called “western duck disease”, it soon spread from western North America to the east of the continent. It then appeared in Australia in 1934, northern Europe and South Africa in the 1960s, New Zealand and East Asia in the 1970s, and to South America around 1980.

Mass die-offs of over 100,000 birds do not occur every year. But when they do, they are almost always in western North America. There have been nine in the US between 1909 and the last one, in 1997. Canada joined the club with three consecutive mass die-offs, in 1995-97, in three different western provinces. The only mass outbreak outside of North America was on the Caspian Sea in what is now Kazakhstan in 1982.

Yet even in the absence of massive deaths, thousands of birds die every year from the disease, but usually go unnoticed. Botulism kills more wild birds than any other disease today.

The Carcass-Maggot Cycle

Botulinum toxin is produced by the bacteria Clostridium botulinum. Like the deadly anthrax bacteria discussed in other posts, C. botulinum survive for long periods, probably years, as dormant spores in the environment, germinating and multiplying only when the conditions are just right. So similar are the two that C. botulinum was initially put in the same genus as anthrax (Bacillus), but it was later found that, unlike B. anthracis, the germinating botulism bacteria cannot survive in the presence of oxygen.

Clostridium botulinum stained with gentian violet. These are gram-positive, rod-shaped, anaerobic bacteria. The small, oval, hollow-looking structures are botulinum spores. Wikipedia

Clostridium botulinum stained with gentian violet. These are gram-positive, rod-shaped, anaerobic bacteria. The small, oval, hollow-looking structures are botulinum spores. Wikipedia

When anaerobic conditions and a protein source are present, botulinum spores may emerge from their sleep and begin dividing, producing a potent neurotoxin in the process. While rotting vegetation or decaying aquatic insects and snails may sometimes provide the necessary proteins for germination, a much more common source is dead waterfowl.

C. botulinum spores are now ubiquitous in wetland environments in affected regions of the world. Ducks and other birds are constantly ingesting the spores from sediment or dead invertebrates as they forage and drink in the water. But the oxygen-perfused body of a living animal cannot support spore germination and so the bacteria have no effect on the birds in all but a very few cases. As birds move from one waterbody to another, they can deposit spores in their feces, helping to colonize new areas.

Duck with characteristic “limberneck” due to botulinum toxicity. Paralysis of the neck muscles prevents the duck from lifting its head, often resulting in drowning. HC Johnstone

Duck with characteristic “limberneck” due to botulinum toxicity. Paralysis of the neck muscles prevents the duck from lifting its head, often resulting in drowning.   HC Johnstone

When a bird dies, it’s carcass quickly becomes an anaerobic environment. Any spores it has consumed may germinate and begin producing toxin. As the body decays, blow flies and flesh flies lay eggs on the flesh and maggots (larvae) emerge within a few days, concentrating toxin as they feed on the duck. These are delicacies for other ducks, which become intoxicated with botulism and soon die. The cycle can repeat until birds leave the site or cooler temperatures reduce fly activity.

A Powerful Toxin

The botulinum toxin is one of the most potent poisons known. It is said that less than 50 grams is enough to wipe out every human being on Earth. The toxin does not appear to have any physiological use to the bacteria that produce it. But its ability to kill the animals that consume it provides a significant advantage for the spread of the bacteria by making a propitious environment for more bacterial growth.

There are eight distinct botulinum toxins, named A through G (including two Type C forms). The only toxin type implicated in the mass die-offs of waterfowl discussed here is Type C toxin, but they all work in similar fashion.

14-year-old boy with botulism. Botulinum Types A and B are most common in people, from consumption of contaminated honey (especially by infants) and improperly preserved foods or wound contaminations. People are highly resistant to the Type C toxin that causes avian botulism die-offs, and the toxin is inactivated by thorough cooking. Wikipedia

14-year-old boy with botulism. Botulinum Types A and B are most common in people, from consumption of contaminated honey (especially by infants) and improperly preserved foods or wound contaminations. People are highly resistant to the Type C toxin that causes avian botulism die-offs, and the toxin is inactivated by thorough cooking.      Wikipedia

Once ingested by an animal, including people, the toxin is absorbed into the bloodstream and makes its way to certain nerve cells in muscles that use the chemical called acetylcholine to communicate a stimulus between neurons. Botulinum toxin interferes with the release of acetylcholine from a stimulated neuron, preventing it from activating neighboring neurons.

Botulinum toxin makes its way to the terminal end of neurons (motor end plate in the image) where they meet the muscle they are meant to stimulate for contraction. This is called the neuromuscular junction. The toxin binds the end of the motor end plate, preventing the release of acetylcholine (ACH in the image) from the neuron into the neuromuscular junction gap, where it would cause the muscle to contract. Slideplayer

Botulinum toxin makes its way to the terminal end of neurons (motor end plate in the image) where they meet the muscle they are meant to stimulate for contraction. This is called the neuromuscular junction. The toxin binds the end of the motor end plate, preventing the release of acetylcholine (ACH in the image) from the neuron into the neuromuscular junction gap, where it would cause the muscle to contract.    Slideplayer

With the muscles unable to contract, the resulting flaccid paralysis often starts in the legs and moves up the body. Affected birds will paddle around a lake with their wings, unable to fly. Many drown when they are unable to hold their head above water. Others suffocate on land when their diaphragm muscle no longer contracts, from dehydration when they can’t get to water, or from predators.

The closely related Clostridium tetani bacteria produces a different type of toxin that causes the opposite reaction. Tetanus toxin allows nerve cells to be stimulated but blocks inhibition pathways that allow the muscles to relax again. This results in contracted muscles that won’t relax, called tetanus. The popular name of lockjaw stems from this effect, with affected people unable to open their mouth. Portrait by Sir Charles Bell

The closely related Clostridium tetani bacteria produces a different type of toxin that causes the opposite reaction. Tetanus toxin allows nerve cells to be stimulated but blocks inhibition pathways that allow the muscles to relax again. This results in contracted muscles that won’t relax, called tetanus. The popular name of lockjaw stems from this effect, with affected people unable to open their mouth.     Portrait by Sir Charles Bell

The Human Role

A large proportion of avian botulism outbreaks are associated with man-made changes to wetlands. The botulinum bacteria have additional preferences besides anaerobic conditions, including temperatures above about 25°C (77°F), slightly alkaline pH of water and sediment, low water salinity, and high amounts of organic matter in the water.

New development in Los Angeles, California. Google Earth

New development in Los Angeles, California.    Google Earth

Anything that alters the above characteristics to be more to the liking of botulinum bacteria can result in avian die-offs. And many human activities do just that:

  • Artificial flooding and drying of wetlands kills plants, invertebrates, and fish. This increases the mass of decaying organic content, leading to reduced oxygen levels and providing nutrients for botulinum spore germination.
  • Shallow waters from drained (and drought-affected) wetlands raise water and sediment temperatures and reduce oxygen levels, both to the liking of botulinum bacteria.
  • Warm water discharged from po
    Wastewater discharge into wetlands alters temperature, salinity, pH, and other characteristics that can precipitate avian botulism die-offs.

    Wastewater discharge into wetlands alters temperature, salinity, pH, and other characteristics that can precipitate avian botulism die-offs.

    wer stations also increases water temperatures as well as decreases salinity through dilution.

  • Raw sewage or fertilizer discharge into wetlands provides nutrients that spark boom-and-bust cycles of organic growth and death that reduce oxygen levels.
  • Massive loss of wetlands to development and agriculture crowd more waterfowl into ever smaller spaces, encouraging the spread of botulism when outbreaks occur.
  • Any cause of bird mortalities under the right conditions can precipitate an avian die-off, providing a ready source of protein for germinating botulinum spores. Starvation, predation, disease, hail storms, pesticide poisonings, even power lines flown into by birds have been implicated in bird deaths that sparked botulism die-offs.

More than Meets the Eye

The botulinum bacteria may prefer certain environmental conditions for their multiplication and toxin production. Yet many sites around the world with seemingly ideal conditions go decades without suffering major botulism outbreaks, even while die-offs occur in nearby wetlands.

In other cases, outbreaks mysteriously occur in what appear to be very unfavorable conditions for the bacteria, including in late winter or early spring, in deep, well-oxygenated lakes and even rivers.

While many massive avian botulism die-offs are associated with heavy environmental impacts of man on wetlands, in other cases the shadow of the human hand appears absent. As man’s impact on nature has continued to increase, there have been no massive avian botulism die-offs since 1997 (though the “normal” background mortality from the disease continues). Clearly the cited risk factors for avian botulism are “guidelines” only.

Blake

Blake

Not surprisingly, given these uncertainties, efforts to prevent avian botulism outbreaks have met with mixed success. Use of aircraft or loud noises to disperse birds from wetlands during outbreaks have met with little success. The effects of draining wetlands during the late summer to disperse spores are unclear. In some cases this seems to result in more invertebrate deaths, which then act as a substrate for the germination of remaining botulinum spores.

Regular removal of carcasses from affected wetlands probably helps when the affected area is a small lake or marsh. But cleanup efforts on larger wetlands (over 400 hectares, or 960 acres) do not appear to significantly reduce duck mortality, possibly because so many carcasses are overlooked. And cleanup is expensive. The Canadian prairies spent over a million dollars in some years on cleanup efforts during the mass die-offs of the mid-1990s.

Despite many advances in our knowledge, avian botulism outbreaks continue to present an enigma. It will likely be a long time, if ever, before we can predict, prevent, or halt the disease with any success.

References

Boere GC, Galbraith CA, and Stroud DA. (eds). 2006. Waterbirds around the world. The Stationery Office: Edinburgh, UK. 960 pp.

Espelund M and Klaveness D. Botulism outbreaks in natural environments – an update. Front Microbiol. 2014; 5: 287.

Friend M, Franson JC, et al. Field Manual of Wildlife Diseases, 1999. USGS: Madison, WI.

Rocke TE & Bollinger TK. (2007). Avian Botulism. In NJ Thomas & DB Hunter (Eds.), Infectious Diseases of Wild Birds. (377-416). Wiley-Blackwell.

Vidal D, Anza I, et al. Environmental Factors Influencing the Prevalence of a Clostridium botulinum Type C/D Mosaic Strain in Nonpermanent Mediterranean Wetlands. Applied and Environmental Microbiology, 2013 Jul; 79(14): 4264-4271.

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