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Crocodile deaths of the Olifants Gorge: Results from a multi-disciplinary, multi-institutional research effort

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Carcass of crocodile that has died from the consequences of pansteatitis

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Dr David Huchzermeyer (right) and Dr Jan Myburgh (centre) with Ms Prudence Shikwambana from SANParks at a field laboratory on the Letaba River

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Barriers to fish movement below the Massingir dam wall, where catfish feeding on concentrated numbers of silver carp also develop pansteatitis

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Sundried silver carp from Lake Massingir - note the oily nature of the flesh

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Typical cyanobacterial bloom at the edge of a water body heavily enriched with nutrient pollutants

By Dr David Huchzermeyer, Veterinary Surgeon and Dr Tony Swemmer, Manager, SAEON Ndlovu Node

 

In the winter of 2008, rangers in the Kruger National Park (KNP) began reporting an alarming high number of dead crocodiles observed in the “Olifants Gorge”, a section of the Olifants River close to the point where the river flows into Mozambique.

Around 170 dead crocodiles were recorded that year, with a similar number of carcasses reported in 2009, and slightly fewer in 2010. The cause of such unnaturally high levels of mortality was not clear, and a significant research effort quickly emerged, involving scientists from a wide variety of organisations - many working voluntarily.

While much has been learnt as a result, and the direct cause of the mortalities is understood, the precipitating factors have yet to be fully understood. And so the informal collaborative research effort around the “crocodile deaths” continues.

Initial speculation included poisoning of the crocodiles by fishermen living downstream in nearby Mozambique, contaminants from the many mines and agricultural areas upstream, the effect of untreated sewerage flowing into the river upstream, and the raising of the wall of Lake Massingir (a large dam in Mozambique, just downstream of the Olifants Gorge).

First significant clue

Autopsies of crocodile carcasses by veterinarians from SANParks and the Faculty of Veterinary Science, University of Pretoria, revealed the first significant clue: the immediate cause of death was pansteatitis, a nutritional disease rarely encountered in wild animals. It results in the hardening of fat tissues, which eventually prevents the free movement of limbs and tails, and ultimately death by starvation or drowning.

But what was the cause of the sudden and severe incidence of this unusual disease in a wild population of crocodiles within a national park? Did it result from the accumulation of heavy metals released by mines; or some unknown response to the complex organic compounds used in pesticides in agricultural areas upstream? Analysis of river water from the Olifants Gorge by Dr Roger Dixon of the South African Police Forensics Service revealed over 1600 artificial compounds in the water, and the effects of almost all of these on crocodiles are unknown to science.

The next clue

Further research by Dr David Huchzermeyer, a veterinarian from Lydenburg who has worked voluntarily on the project, provided the next clue - the cause of the pansteatitis. The disease has been described from many species of captive and farmed animals, including fish. In all cases the condition has been associated with unsuitable diets containing either rancid fats or high levels of fish oils.

Fish oils contain high levels of polyunsaturated fats. Many of these have vital functions in organelle and cell membranes, which is the reason why the consumption of polyunsatured fats by humans is promoted by nutritionists. However, these compounds are unstable and can break down into harmful substances through the process of oxidation.

Animals have complex anti-oxidant mechanisms to prevent the breakdown of these unstable fatty acids, the most important of which involve vitamin E. High dietary intake of polyunsaturated fatty acids in fish is known to lower tissue vitamin E levels, leading to greater risk of oxidation of lipids and the formation of harmful free radicals. Analysis of blood sampled from dead and dying crocodiles by Dr Jan Myburgh of the University of Pretoria, indicated very low concentrations of vitamin E.

While excessive consumption of polyunsaturated fatty acids may have been the reason for the low vitamin E levels in the Olifants Gorge crocodiles, the same effect could be caused by the consumption of certain toxins, which can damage the phospholipids of organelle and cell membranes. These toxins include certain metals and organic compounds, particularly those that undergo redox cycling (such as iron and copper, both mined alongside the Olifants River, upstream of KNP).

However, according to Dr Huchzermeyer there is no evidence that heavy metals or organic pollutants will cause actual pansteatitis. Furthermore, analysis of the river water in the gorge at the time of the deaths, conducted by Philip Kempster of the Department of Water Affairs, revealed that no metals were at a toxic concentration. Likewise, analysis of persistent organic pollutants by Prof. Henk Bouwman (North-West University) revealed that these pollutants were not present at concentrations thought to be toxic. Similarly, analyses of toxins within crocodile tissues, some of these done by laboratories in Norway, Japan and the USA, also indicated that concentrations of all these pollutants were not high enough to cause disease.

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Dr David Huchzermeyer (second from left) demonstrating pansteatitis in catfish to Dr Jan Myburgh (left) of the University of Pretoria and Skukuza state veterinarians Drs Roy Bengis (right) and Lin-Mari de Klerk

The assimilation of polyunsaturated fatty acids seemed the most likely trigger for the unusual disease. In other words, the diet of the crocodiles must have become unbalanced, with too much intake of prey or carrion that was rich in polyunsaturated fatty acids. Some of these fatty acids are essential nutrients, and consumption of these fats is beneficial to the health of humans and animals in general, provided they form part of a balanced diet. In contrast, Dr Huchzermeyer suspected that the diet of crocodiles and catfish in the Olifants Gorge became unbalanced with an excessive consumption of polyunsaturated fatty acids, and that this outstripped the intake and availability of antioxidants required to keep the assimilated fatty acids from oxidising.

Were the catfish to blame?

Further autopsies by Dr Huchzermeyer revealed that the African sharptooth catfish, Clarias gariepinus (Burchell), a dominant fish in that part of the river and thought to be an important part of the crocodiles’ diet, also showed symptoms of pansteatitis. Dead and decaying fish may contain high levels of oxidised (rancid) fatty acids and ingestion of such dead fish is known to cause pansteatitis. Fish die-offs had not been a feature in the Olifants Gorge preceding the crocodile mortalities of 2008 and 2009, but may have simply been overlooked due to the remoteness of the Olifants Gorge.

However, the shift in blame soon moved from dead catfish to a more unusual source of crocodile food. Comparison of the fatty acids of pansteatitis-affected wild crocodiles, healthy wild crocodiles and farmed crocodiles indicated that rancidity of dietary fats was not the cause of pansteatitis in crocodiles in the Olifants Gorge. In other words, the consumption of dead fish by the crocodiles was an unlikely cause for the disease. This was corroborated by fatty acid analyses of pansteatitis-affected wild catfish, healthy wild catfish and pansteatitis-affected farmed catfish where the pansteatitis was known to have been induced by rancid dietary fat.

Could algal blooms have been the cause?

Analysis of fat tissue from both crocodiles and catfish suffering from pansteatitis in the Olifants Gorge, by Dr Garry Osthoff and co-workers at the University of the Free State, reflected a higher intake of very-long-chain polyunsaturated fatty acids, particularly docosahexaenoic and eicosapentaenoic acid in pansteatitis-affected crocodiles and catfish. The source of these particular fats is not dead fish, but rather phytoplankton (small single-celled algae that float around in rivers and dams). Yet crocodiles and catfish do not feed directly on phytoplankton.

Nutrient pollution has been a serious problem in the Olifants catchment for many years and artificial impoundments are known to trap these nutrients, leading to the process of eutrophication (an excessive supply of naturally occurring nutrients). Eutrophication typically results in population explosions of phytoplankton, which are able to exploit the oversupply of nutrients such as phosphates and nitrates.

Lake Massingir, just downstream of the Olifants Gorge, is known to be eutrophic and is subject to seasonal phytoplankton blooms. Crocodiles do not consume phytoplankton, but certain fish species do, and fish that feed almost exclusively off phytoplankton can assimilate very high levels of polyunsaturated fatty acids in their tissues. If these are then consumed by the crocodiles, abnormally large amounts of polyunsaturated fatty acids could accumulate in the crocodiles.

Analysis of the food web in the Olifants Gorge by Dr Stephan Woodborne (with the CSIR at that time) indicated that this was indeed the case. Results of his stable isotope analyses showed that crocodiles and catfish affected with pansteatitis were consuming nitrogen from a different source compared to healthy animals from the same site. As nitrogen enters the food chain via phytoplankton, this provided further evidence that a trophic shift (or rather a shift in diet) was responsible for the incidence of pansteatitis in both crocodiles and catfish in the Olifants Gorge. The same trophic shift was identified in tigerfish from the Olifants Gorge, but this obligatory piscivorous species appears to have evolved sufficient antioxidant defences to tolerate this.

And the (current) villain is ...

The change of focus to trophic shift and eutrophication led Dr Huchzermeyer to the latest (and still current) villain in the crocodile death saga: the silver carp, Hypophthalmichthys molitrix. Native to China, the silver carp was introduced into Lake Massingir intentionally to improve the fisheries potential of this lake. Around the same time silver carp accidently escaped into the middle stretches of the Olifants River from a training college in South Africa. The species became well established in the lower Olifants River.

Silver carp are obligate filter feeders and thrive on phytoplankton blooms in Lake Massingir, from which they assimilate uniquely high levels of polyunsaturated fatty acids into their fat tissues. It is speculated that crocodiles and catfish in the Olifants Gorge consume large numbers of silver carp where these fish congregate seasonally to spawn at fish barriers in the gorge. The flooding and subsequent hydrodynamic changes that occurred in the Olifants Gorge after the sluice gates in the Massingir dam wall were raised in 2007, may have made it possible for crocodiles and catfish to access abnormally large numbers of silver carp. Excessive consumption of polyunsaturated fatty acids would have resulted, leading to the pansteatitis deaths in the following years.

The outlook ...

Pansteatitis is not rapidly fatal to catfish, and affected fish may survive for long periods (although the effect of predation on sick fish is not known). Crocodiles that are mildly affected are likely to survive from season to season, but damage to their fat tissues may be cumulative (as in the case of catfish). The question remains whether the disease will continue to decimate crocodiles in the Olifants Gorge. Differing levels of nutrient pollution, light intensity as well as increases in atmospheric carbon are likely to have an impact on the intensity and composition of phytoplankton blooms in Lake Massingir . This will influence the level of polyunsaturated fatty acid assimilation by silver carp.

Furthermore, the physical appearance of the Olifants Gorge changes from year to year according to flood events and the level of subsequent siltation. These seasonal hydrodynamic changes may create new barriers to the migration of spawning silver carp, affecting the ease with which crocodiles and catfish are able to prey on these fish. With continuing high levels of nutrient pollution from the catchment accumulating in the dam, it is unlikely that the crocodile mortalities of 2008 and 2009 were a once-off event.

With so many variables it is difficult to predict future mass mortality events associated with pansteatitis. But the cumulative effect of sub-lethal pansteatitis lesions, as in the case of catfish, can be expected to lead to a gradual and persistent weakening of the surviving crocodile population.

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