FAT NECROSIS IN FISH: RELEVANCE OF HYDRODYNAMIC CHANGE AND POLLUTION TO THE AQUATIC FOOD CHAIN IN THE KRUGER NATIONAL PARK, SOUTH AFRICA

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1 FAT NECROSIS IN FISH: RELEVANCE OF HYDRODYNAMIC CHANGE AND POLLUTION TO THE AQUATIC FOOD CHAIN IN THE KRUGER NATIONAL PARK, SOUTH AFRICA David Huchzermeyer Sterkspruit Veterinary Clinic University of Pretoria WRC Consultancy Project K8/948

The study forms part of the multidisciplinary investigation into the crocodile mortality in the KNP under the auspices of the Consortium for the Restoration of the Olifants Catchment (CROC) With

2 The study forms part of the multidisciplinary investigation into the crocodile mortality in the KNP under the auspices of the Consortium for the Restoration of the Olifants Catchment (CROC) With funding and assistance from: Water Research Commission Sterkspruit Veterinary Clinic IDEXX Laboratories SAN Parks University of Pretoria South African Veterinary Foundation South African Police forensics laboratory KNP

3 History of crocodile deaths Lake Loskop increasing deaths since 2003 Olifants Gorge high mortality in 2008 following raising of the sleuces of Lake Massingir in 2007 resulted in flooding of the Olifants Gorge. Each year since 2008 the mortality of crocodiles in the Olifants Gorge has declined but a low level persists Sabiepoort the gorge at the inlet to Lake Corumana Low levels of mortality recorded since 2010

4 Cause of deaths in crocodiles Pansteatitis

5 Pansteatitis Inflammatory reaction that accompanies the generalized necrosis of fat Described from many species of warm and cold blooded animals including fish Generally regarded as a function of polyunsaturated fat consumption and dietary vitamin E intake May be initiated by exogenous factors

6 Consumption of fish Pansteatitis is associated with the consumption of large amounts of fish, particularly if no longer fresh Only a single large scale fish mortality was recorded in the Olifants Gorge during the study period Photo Reuters

7 Process leading to pansteatitis Redox cycling of various compounds can result in damage to polyunsaturated lipids causing release of lipid hydroperoxides Lipid hydroperoxides decompose to highly reactive lipid free radicals Lipid free radicals promote further peroxidation of polyunsaturated lipids and initiate damage to cell and nuclear membranes Vitamin E protects polyunsaturated lipids from damage caused by lipid free radicals

localities within and outside of Kruger National Park.

8 Sampling During the period June 2009 to June 2011, 285 specimens of C. gariepinus were examined during 17 sampling episodes from various localities within and outside of Kruger National Park. Fish were subjected to detailed autopsies and subsequent histological examination of the organs.

9 Sharptooth catfish Clarias gariepinus: are benthic scavengers locality specific differences in food sources Fat deposition reflects higher food abundance at certain sampling sites

10 Stomach and intestinal content of C. gariepinus Olifants Gorge predominantly fish remnants from fairly large fish Olifants River at Ngotso and Mamba weir predominantly Sycamore figs Gorge on Mozambique border almost exclusively silt and associated detritus Reenvoel dam predominantly plant, invertebrate and insect detritus Van Ryssen Dam exclusively fish

11 Olifants Gorge C. gariepinus with steatitis cross section of mesenteric fat reactive spleen

12 Steatitis in fat of C. gariepinus from Lunsklip Fisheries

13 Steatitis in mesenteric fat of C. gariepinus from Olifants Gorge July Mesenteric fat body 2010 Cross section of mesenteric fat body

14 Pansteatitis in C. gariepinus from Olifants Letaba confluence July 2010 Mesenteric fat Pectoral fat Intermuscular fat Fat Brain Lesions in fat

15 Normal fat cells Positive staining ceroid pigment in ruptured adipocytes and macrophages in mesenteric fat of C. gariepinus OG November 2009 HE X 40 GAF X 40

16 Pansteatitis in the Olifants Gorge fish was not correlated to either: Age or Fat to body mass ratio Otolith section of 4 year old fish from OG Otolith section of 19 year old fish from OG

17 Relative ages of fish sampled Sampling site Age range all fish Age range of fish with steatitis Olifants Gorge Mamba Weir Engelhard Dam Sabiepoort Reenvoel Dam 1 19 Van Ryssen Dam 1 13 Levuvhu River 1 9 Crocodile River 1 8 Lunsklip Fisheries

18 Mean mesenteric adipose tissue mass relative to body mass

20 Steatitis prevalence as percentage of sampled sharptooth catfish from Olifants Gorge during the period % Steatitis Time (days) Time (days since start of sampling) Correlation coefficient: r = 0.87 Significance of model: p = 0.02

21 Prevalence of macroscopic steatitis lesions in negative and positive reference populations of sharptooth catfish Date Sampling site % fish with steatitis Total fish sampled November 2009 November 2009 Reenvoel Dam Lunsklip Fisheries January 2011 Reenvoel Dam

22 Summary of field samplings (June 2009 to June 2011). An increasing prevalence of fat necrosis and steatitis was recorded in C. gariepinus sampled from the Olifants River gorge Over 60 % of C. gariepinus collected during the most recent sampling from the Olifants Gorge were suffering from steatitis. A decline in amount of fat stored by C. gariepinus was noted with repeat samplings from the Olifants Gorge Steatitis has been confirmed in C. gariepinus collected from the Sabie River in the Sabiepoort at a similar prevalence to that found in the Olifants Gorge. A high prevalence of nutritionally induced steatitis was identified in a farmed population of C. gariepinus. This provided the study with valuable comparative pathology.

23 C. gariepinus Olifants Gorge July 2010 & January 2011 Nile crocodile Olifants Gorge August 2009

24 Summary of experimental work with C. gariepinus Steatitis in C. gariepinus is not rapidly fatal. Behavioural changes were observed in affected fish Steatitis could not be induced over a 14 month period by keeping C. gariepinus over Olifants Gorge sediments in experimental tanks Steatitis lesions and reactive spleen retained in captive C. gariepinus 11 months after removal from inciting cause and dietary correction.

be able to mobilize fat from the affected tissue, explaining muscle wasting seen in

25 Steatitis lesions do not heal over time in C. gariepinus Once steatitis is present in the adipose tissues, fish appear to no longer be able to mobilize fat from the affected tissue, explaining muscle wasting seen in some individuals. If affected fish continue to feed they are able within limits to deposit new fat adjacent to the steatitis fat.

26 Tiger fish samplings Tiger fish are obligate piscivorous predators Pansteatitis could not be demonstrated in tiger fish sampled from the Olifants Gorge during June 2011

27 Olifants River catchment - heavily impacted by human activity including: coal fired electricity generation industrial and urban wastewater discharges, agricultural practices mining water impoundments Map: Heath R, Coleman T, Engelbrecht J (2010) WRC Report No. TT 452/10

Anthropogenic impact on the Olifants River catchment (Ashton P J 2010) De Villiers S, Mkwelo S T 2009) covers some 74 500 km 2 home to about 8% of South Africa s population approximately 90% of

28 Anthropogenic impact on the Olifants River catchment (Ashton P J 2010) De Villiers S, Mkwelo S T 2009) covers some km 2 home to about 8% of South Africa s population approximately 90% of the country s saleable coal is mined in this catchment used to generate 55% of South Africa s electricity, large areas of the landscape have been changed by afforestation, agriculture and mining

29 Added concerns of eutrophication (Heath R, Coleman T, Engelbrecht J 2010) Huge increases in urban wastewater discharge and already high nutrient run-off from agricultural practices country s second largest irrigation scheme. numerous water impoundments, including 38 major dams in the Olifants catchment

30 Changing water quality may cause sediment bound contaminants to become bio-available and bio-accumulate in fish tissues. Coetzee L, du Preez H H, van Vuuren J H J 2002 contamination of surface waters in the catchment accumulation within sediments through adsorption and precipitation processes large dams act as traps for sediments, nutrient toxins and heavy metals

31 Olifants Gorge Mozambique border and Massingir Dam

32 Lunsklip Fisheries Captive C. gariepinus fed an excess of fat rich trout slaughterhouse waste Fish show classical nutritionally induced pansteatitis

33 Conclusion Large dams in the catchment act as traps for sediments, nutrient toxins and heavy metals and are regarded as the epicentre of recent mortalities of fish and crocodiles (Heath R, Coleman T, Engelbrecht J 2010) In the KNP, pansteatitis in both catfish and crocodiles has been observed in areas where the natural habitat has been drastically altered as a result of damming of rivers, and the associated deposition of large clay deposits is a potential source of pollutants. There are numerous references in the literature linking lipid peroxidation to pollutants in the aquatic environment, but little has been published linking these effects to pansteatitis, which is still regarded as a nutritional disease

34 Summary Pansteatitis occurs in both crocodiles and in C. gariepinus in the Olifants Gorge and in the Sabiepoort C. gariepinus is a benthic scavenger and is likley to be an important link in the development of pansteatitis in the crocodiles The association of steatitis with man made lakes in this known polluted catchment suggests that hydrodynamic change and pollution are the main drivers of this condition

K D A Huchzermeyer 1,2, G Osthoff 3, A Hugo 3 and D Govender 4

K D A Huchzermeyer 1,2, G Osthoff 3, A Hugo 3 and D Govender 4 Comparison of the lipid properties of healthy and pansteatitis-affected African sharptooth catfish, Clarias gariepinus (Burchell), and the role of diet in pansteatitis outbreaks in the Olifants River in