FAT NECROSIS IN FISH: RELEVANCE OF HYDRODYNAMIC

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 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
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
Cause of deaths in
crocodiles
• Pansteatitis
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
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
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
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.
Sharptooth catfish Clarias gariepinus:
• are benthic scavengers – locality specific
differences in food sources
• Fat deposition reflects higher food
abundance at certain sampling sites
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
Olifants Gorge – C. gariepinus with steatitis
cross section of mesenteric
fat
reactive spleen
Steatitis in fat of C.
gariepinus from
Lunsklip Fisheries
Steatitis in mesenteric fat of
C. gariepinus from Olifants Gorge July
2010
• Mesenteric fat body
• Cross section of
mesenteric fat body
Pansteatitis in C. gariepinus from Olifants Letaba
confluence July 2010
Mesenteric fat
• Pectoral fat
Intermuscular fat
Lesions in fat
Fat
Brain
Normal fat cells
HE X 40
Positive staining ceroid pigment
in ruptured adipocytes and
macrophages in mesenteric fat of
C. gariepinus OG November
2009
GAF X 40
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
Relative ages of fish sampled
Sampling site
Age range all fish
Age range of fish with steatitis
Olifants Gorge
1 – 19
1 – 19
Mamba Weir
1 – 12
12
Engelhard Dam
1 – 11
3 – 11
Sabiepoort
Reenvoel Dam
1–8
1 – 19
4–8
Van Ryssen Dam
1 – 13
Levuvhu River
1–9
Crocodile River
1–8
Lunsklip Fisheries
5 – 13
5 - 13
Mean mesenteric adipose tissue mass relative to body mass
Steatitis prevalence as percentage of sampled sharptooth
catfish from Olifants Gorge during the period 2009-2011.
70
65
60
% Steatitis
55
50
45
40
35
30
25
0
100
200
300
400
500
600
700
Time start
(days)
Time (days since
of sampling)
Correlation coefficient: r = 0.87
Significance of model: p = 0.02
800
Prevalence of macroscopic steatitis lesions in negative and
positive reference populations of sharptooth catfish
Date
November
2009
Sampling site
Reenvoel
Dam
November
Lunsklip
2009
Fisheries
January 2011 Reenvoel
Dam
% fish with
steatitis
Total fish
sampled
0
23
66
21
0
13
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.
C. gariepinus Olifants
Gorge July 2010 & January
2011
Nile crocodile Olifants Gorge
August 2009
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.
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.
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
Olifants River catchment - heavily impacted
by human activity including:
coal fired electricity generation
industrial and urban wastewater discharges,
agricultural practices
water impoundments
mining
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 km2
• 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
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
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
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
Olifants Gorge Mozambique
border and Massingir Dam
Lunsklip Fisheries
• Captive C. gariepinus fed an excess of fat rich trout
slaughterhouse waste
• Fish show classical nutritionally induced pansteatitis
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
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