Pansteatitis in catfish: consequences of nutrient

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
• 8% of South Africa’s
population
• Mining of 90% of the
country’s saleable coal
• used to generate 55% of
South Africa’s electricity,
• Landscape
alterations 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
• 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 lipiddamaging 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 antioxidant 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 postmortal 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 radicalmediated damage, there is
potentially an increased risk of
radical attack on human
tissues after consumption of
such fish products
Smoked silver carp – Lake Massingir