4. Bioaccumulation - Lecture notes 4 PDF

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Gary Caldwell...

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Trophic transfer and bioaccumulation of phycotoxins To bioaccumulate literally means to accumulate in a biological system Bioaccumulation is divided into bioconcentration and biomagnification: -

Bioconcentration considers uptake from the non-living environment e.g. direct uptake of lead in fish from polluted rivers Biomagnification, or bioamplification describes uptake through the food chain e.g. accumulation of PCBs and DDTs in birds of prey from eating contaminated rodents

Chemicals in biological systems have biological half lives i.e. how long they will stay in that system until they are lost, excreted, degraded or react into something different If the input of a toxic substance to an organism is greater than the rate at which the substance is lost, the organism is bioaccumulating. Summarised in the following highly simplified equation:  

Toxin in – Toxin out = > 0  therefore it is bioaccumulating However, this equation belies much biological detail e.g. detoxification

Storage and production of toxins within algal cells Some toxins may be produced as grazing deterrent e.g. domoic acid Most toxins are produced constitutively (synthesised at a constant rate regardless of physiological demand or concentration of a substrate) therefore, poses serious risk of autotoxicity. But how do algae avoid self-toxicity? -

Neurotoxins – attack nervous system are common chemicals Algal cells do not have neurotoxin They are still toxic E.g. cytotoxicity

A number of possible mechanisms exist to avoid self-toxicity… -

Compartmentation o Intracellular partitioning of cellular substances and metabolic activities by membranes o Basically lock it away o E.g. saxitoxins and oxadaic acid are compartmentalised in the chloroplasts of Gonyaulax and Prorocentrum respectively o Toxins stored securely o Do not affect other cell functions o If needed, can be released ‘from compartment’

Accumulation of algal toxins in zooplankton Baltic Sea zooplankton accumulate nodularin from cyanobacteria. Concentrations correspond with zooplanktivorous fish. Baltic zooplankton also known to accumulate microcystins. Cyanotoxins also found in mussels, fish and ducks. Variation in bioaccumulation through time and between species Gross accumulation in the ecosystem can be an important aspect to look at. Accumulation of PSP toxins -

Any grazer size class could be initial vector for PSP toxins in food web

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Extent of PSP transfer to zooplankton determined by complex interaction among several factors, including toxic cell and grazer abundance, algal toxin cell quota, and zooplankton community composition Key trends = cells that are very toxic have very poor bioaccumulation, cells that are less toxic have a higher bioaccumulation This could be because grazers choose not to consume toxic cells But instead consume more cells of less toxic causes higher bioaccumulation Some copepods deliberately consume high toxic cells so they build up PSP toxins in their own body as they can tolerate up to a certain amount of toxins. But this also deters predators. This then suggests fish can detect toxins in copepods before consuming and choose to spit those out which have high toxicity

Main findings: constructed a toxin budget for zooplankton finding that most toxin is released into environment where it is less harmful through excretion. Some toxins are built up in the body and not excreted out – selective accumulation of toxins? Need to consider the following factors when thinking about toxin accumulation: -

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Sloppy feeding – can not assume the amount of toxins found in algae are the same amount consumed. A lot of cell content is lost to environment through sloppy feeding of copepod. Defecation – transfer of non-ingested toxins back into environment Feeding mode – filter feeders have less loss of cell contents Feeding rate – some accelerate feeding rate to accumulate toxins to prevent predation Detoxification – Biochemical mechanisms within organisms that to a certain degree detoxify the compounds through breaking them down or changing the chemical structure Gut retention time – Amount of time between copepod ingesting algal cell to it being voided out through faeces. This means longer gut retention time the longer the toxin has to get into rest of body. Dilution effects – dilution of toxin with non-toxic cells. Always other species present in algal blooms so copepods can switch the cell they are feeding on from ‘bad’ toxic cell to other cells within the blooms that they selectively choose. Selectively avoid toxic cells. Body retention – how long copepod can retain toxins in body for. Different to gut retention. Is toxin lipophilic, hydrophobic? Rather go into oils or water? If water it is easy to void out of body through excretion. If it is a lipid binding toxin this is much harder to excrete. Ovaries are very lipid rich (for yolk) this could be an issue in terms of it being toxic Temperature – Impact biochemical speed of enzymes. Impact activity of animal itself. Impact gut retention time etc…

Maneiro et al. (2005) Main findings show copepods accumulate 4.8% of ingested domoic acid despite detoxifying >60% of toxin. Some form of detox process in operation – not sure what? Accumulation of toxins in macroinvertebrates Filter feeding bivalves (mussels, oysters, clams) are classic examples of toxin bioaccumulation – termed as vectors of shellfish poisoning. Human intoxications (other than ciguatera) generally come from eating bivalves. Can eliminate toxin load (in some circumstances) if ingestion of toxins ceases (time dependent). Harvested molluscs can depurate (to cleanse or purify) for a period of time before being sent to market – the effectiveness of this is questionable. -

Depurate through putting into tanks of very clean filtered seawater for 24-72 hours

Oysters are a well-known vector of norovirus/cholera to humans. Depuration helps prevent these infections but little evidence to support its effectiveness against algal toxins.

Epimerisation is a type of asymmetric transformation in organic molecules. Can occur in dinoflagellate or any organism that acquires the toxin. Can have a significant impact on toxicity of phycotoxins.

Bivalves can epimerise STX by switch H and OSO-3 on the no. 11 position. Acid hydrolysis separates the SO-3 group from no. 21 = toxicity increase x6 Stomach is acidic and acid hydrolysis can occur after you eat shellfish Not all filter feeders accumulate toxins to the same extent – even within the same species… WHY??? Bricelj et al. (2005) Sodium channel mutation leading to saxitoxin resistance in clams increases risk of PSP. Nature 434, 763-767 Study used soft shell clams (Mya arenaria) Known that Mya from areas with red tides have much greater resistance to PSP and accumulate PSP at a greater rate – very real danger of human intoxication. Chose two study sites – one prone to have red tides and the other an estuary with no red tides. This proved the above statement – this was because clams from no red tides area are less able to burrow so suffered some physiological stress causing a higher mortality. Why is this the case? % blocked nerve fibres is greater in the clams from no red tides area. Up to 100-fold increase in SRX needed to block sodium channels of red tide calms. Therefore, red time clams are much more resistant to STX effects. STX resistance caused by a single nucleotide mutation in the outer pore loop of Domain II of the Na + channel – replacing glutamic acid with aspartic acid. Algal biotoxin accumulation in non-filter feeding invertebrates: -

Domoic acid – identified in cephalopods off Portuguese coast high concentrations in digestive glands – likely accumulated from feeding on crabs, bivalves and fish. PSP – accumulation in shore crabs (Japan) – accumulated toxins in hepatopancreas in proportion to the amount of toxic mussels they ingested Carnivorous gastropods in Chile – highest toxicity about 5 months after the bloom DSP accumulated in edible crab Cancer pagarus. Toxins only accumulate in digestive organs (hepatopancreas)

Accumulation of toxins within fish

Accumulation of microcystin in silver carp (Hypophthalmichthys molitrix) -

Fish fed exclusively with toxic Microcystis at a density of 6x109 algal cells L-1. LD50 of microcystin-LR of 270μg kg-1 body weight, therefore strong resistance to microcystis. Microcystin concentrations in muscle and liver were 1.57μg kg-1 and 4.28μg kg-1 fresh weight (within safe limits for human consumption) If not cleaned properly or something not gone right in preparation can become seriously ill. As liver has so much more toxins than muscle. Silver carp may be used in cyanobacterial bloom control.

Nodularin accumulates in Baltic Sea trout liver resulting in a loss of liver architecture -

Cells begin to swell up Nucleus structure aren’t as structured Architecture isn’t as clear

Accumulation of domoic acid in sardines (Portugal) -

Annual problem – toxins present between April and October, therefore toxic conditions may persist in sardines for a lengthy period of time. Is likely a reflection on the ability of domoic acid producing diatom blooms to persist within the environment. Accumulation level varied from organ to organ No DA found in muscle, so safe for human consumption – but requires careful preparation of the fish

Accumulation of PSP toxins in mackerel Scomber scombrus -

Atlantic mackerel are known to be lethal vectors of PSP toxins to predators Mackerel appear to retain toxins year-round Toxins accumulate in liver with progressive accumulation throughout the fish’s life Consumption of ‘toxic’ zooplankton the most likely cause But the health of the fish is actually being damaged by the toxin over time Only choose smaller fish to eat as older larger fish have a higher amount of toxin in the liver than flesh o Although this is not an issue so long as fish is prepared properly

Accumulation of ciguatoxin in food web Origin at bottom of food chain, in dinoflagellates; Gambierdiscus toxicus, Prorocentrum lima, Ostreopsis sp. and Coolia montis. Triggerfish feeding on sea urchins can be incredibly toxic as urchins highly concentrate ciguatera. -

CTX also accumulates in other invertebrates e.g. giant clam and trochus gastropod

Incidental consumption as can’t avoid dinoflagellates. Passed on from herbivore to carnivore to humans. At each stage more and more accumulates. Also a link to the palatability of macroalgae on which dinoflagellate grows: -

How tasty seaweed to herbivores depends on how much toxin is consumed If you produce compounds that make you taste bad, you’ll be predated on less so dinoflagellates found on tastier seaweed will accumulate more Potential link to hurricanes? o Damage to coral structure o Coral rubble deposited on seabed o This is a good habitat for CTX so thrive on it

Lab feeding trial with unicorn fish – fed Gambierdiscus in gel packages (89 cells/g)

CTX accumulation in muscle following 76 feeds over 16 weeks -

Steady decline in blood levels of CTX over the day CTX in tissue plateaus out over the day and potentially increases a little bit at the end of the day Potential transfer of CTX from blood into tissue over the day...