Pansteatitis in Catfish: Consequences of Nutrient Pollution and Man-Made Hydrodynamic Change for the Kruger National Park

Pansteatitis in catfish: consequences of nutrient pollution and man-made hydrodynamic change for the Kruger National Park

David Huchzermeyer

Sterkspruit Veterinary Clinic University of Pretoria WRC Consultancy Project K8/948 Clarias gariepinus • Benthic omnivores • Stalking predators

• Concentrated feeders utilising specific food sources exclusively, when abundant (Bruton 1979)

• With easy access to prey the most common species of suitable size is taken most frequently (Willoughby & Tweddle 1978)

• Powerful and fast swimmers when hunting in rapids (Bell-Cross 1976) Massingir spillway Feb 2013 – 31% Anthropogenic impact on the Olifants River catchment (Ashton P J 2010) De Villiers S, Mkwelo S T 2009)

• 74 500 km2 • Landscape • 8% of South Africa’s alterations by population afforestation, • Mining of 90% of the country’s saleable coal agriculture and • used to generate 55% of mining South Africa’s electricity, Added concerns of eutrophication (Heath R, Coleman T, Engelbrecht J 2010)

• Huge increases in • numerous water urban wastewater impoundments, discharge and including 38 major • already high nutrient dams in the Olifants run-off from catchment agricultural practices • country’s second largest irrigation scheme.

• steatosis – death of fat cells • steatitis – inflammation following death of fat cells The biochemical basis of the lesion that appears in the fat tissues is the end process of a lipid- damaging chain reaction set in motion by oxidative stress

crocodile catfish Pansteatitis • a complex dietary disease • initiated by oxidative stress caused by: 1. consumption of oxidised (rancid) polyunsaturated fats – dead and rotting fish or

2. over-consumption of fresh polyunsaturated fats – change in diet to oil rich fish species in animals poorly adapted to such a diet Other causes of oxidative breakdown of phospholipids follow similar biochemical pathways • Redox-cycling of metals and organic compounds is known to initiate lipid peroxidation - no conclusive evidence of implication in pansteatitis • Vitamin E is the major chain breaking anti- oxidant protecting from oxidative damage - deficiency leads to propagation of lipid peroxidation and may contribute to the development of pansteatitis Episodic oxidative stress • Pathology in fat tissues with pansteatitis persists long after the oxidative insult – granulomatous reaction in the fat tissues analogous to scar formation • Antioxidant parameters return to normal once the animal has survived the initial insult • Vitamin E values return to normal following recruitment from other tissues and dietary sources

• Pathology is mainly restricted to the adipose tissues In the Olifants Gorge • Pathology in the catfish indicated exposure to episodes of oxidative stress

• No pathology was found indicative of continuous oxidative stress

• No correlation between pansteatitis and metal bio-accumulation Did pollution play a role in pansteatitis in the Olifants Gorge?

• Bio-accumulation of xenobiotics in fish from the Olifants Gorge has not been ruled out

• A link between xenobiotics and pansteatitis could not be demonstrated How did pollution play a role in pansteatitis in the Olifants Gorge? • Unacceptably high phosphate values were measured repeatedly in the Olifants River prior to 2004 and occasionally since then

Source J. Venter SANParks • Phosphates trapped in Lake Massingir have driven eutrophication of the lake Phytoplankton and pansteatitis

• Phytoplankton – a rich source of PUFAs, particularly omega 3 fatty acids • Filter feeding fish species assimilate omega 3 fatty acids from phyto- and zooplankton

• Many animals have dietary requirements for PUFA’s, but these fatty acids are unstable and easily oxidise requiring adequate tissue anti-oxidants

• Tissue vitamin E levels are inversely proportional to PUFA intake Consequences in the OG

Dietary assimilation of PUFAs consumes tissue vitamin E

What if excessive amounts of PUFAs are consumed?

Once tissue vitamin E is depleted PUFAs oxidise setting in motion a chain reaction that leads to pansteatitis Massingir Dam • Hydrodynamic change in the Olifants Gorge has created bottle-necks where catfish and crocodiles episodically feed on migrating fish species that would not normally be consumed in such large numbers.

• It is speculated that in the Olifants Gorge the alien silver carp is one such species

Hypophthalmichthys molitrix

• Obligate pellagic filter feeder known to thrive on cyanobacterial blooms • An alien invasive fish outside of its home range in East Asia occupies an ecological niche filled by no indigenous fish species in South Africa • Known to assimilate PUFAs at levels similar to marine fish • Known to school and migrate out of still waters of lakes into deep fast flowing water to spawn for a short period during each summer • Known to occur in Lake Massingir and the Olifants River Contribution of other factors 1. Other fish species? Improbable that non-migratory phytoplankton-feeding species would play a role, as crocodiles and catfish are unlikely to consume quantities sufficient to overwhelm their anti-oxidant defences. 2. Consumption of dead fish during periodic fish kills and from fishermen’s nets? Comparative fat analyses from captive catfish fed rancid fish provides argument against this

3. Redox-cycling xenobiotics? No conclusive evidence that this can lead to pansteatitis Findings of this and related studies indicate that this is not happening in catfish in Olifants Gorge (see Dixon and Huchzermeyer 2013) Epidemiological factors in the Olifants Gorge

1. Phosphate pollution

2. Water retention by Massingir Dam has created a nutrient trap

3. Phytoplankton growth and eutrophication

4. Introduction of an alien filter feeding fish species 5. Barriers to fish migration Pansteatitis in the Sabiepoort - a conundrum?

• Pansteatitis has been identified in both catfish and crocodiles in the Sabiepoort but a detailed analysis of fat composition and stable isotopes has not been done. • Silver carp have not been confirmed from Lake Corumana but are known to occur in the Sabie River downstream of the lake

• Consumption of dead, rancid fish cannot be ruled out Pansteatitis in the Olifants Gorge • Aetiology is complex and has a dietary basis linked to piscivory • Prevalence may vary from year to year • Fatty acid composition and quantity of fat deposited by silver carp and other fish is likely to vary depending on the intensity and type of phytoplankton that is dominant in the blooms they consume • Sources of nutrient pollution of the Olifants River need to be addressed • Phytoplankton blooms in Lake Massingir should be monitored. Human health concerns • The in vivo lipid-stabilising function of vitamin E extends beyond the life of the animal and is important in the storage stability of meat products.

• The risk of post- mortal oxidative lipid breakdown (rancidity) is magnified in fish as a result of the high polyunsaturated fatty acid content of fish flesh. Smoked silver carp – Lake Massingir • In many parts of Africa, lack of cooling facilities and poor sanitary conditions lead to rapid deterioration of harvested fish. • Smoked freshwater fish, such as those from Lake Massingir, are a popular product and may be stored for several weeks and shipped long distances before being consumed.

Are fish exposed to oxidative stress safe for human consumption?

• Oxidative damage to phospholipids is believed to be the basis of many diseases

• Where vitamin E levels in tissues are already low as a result of in vivo radical- mediated damage, there is potentially an increased risk of radical attack on human

tissues after consumption of Smoked silver carp – Lake Massingir such fish products