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Biology

Big Fish Eats Little Fish: Biomagnification of Natural Toxins

Paper: Mak, Y. L.; Wai, T-C.; Murphy, M. B.; Chan, W. H.; Wu, J. J.; Lam, J. C. W.; Chan, L. L.; Lam, P. K. S. Pacific ciguatoxins in food web components of coral reef systems in the Republic of Kiribati. Environ. Sci. Technol. 2013. doi: 10.1021/es403175d

Ciguatoxins: Natural poisons hidden in algae

These days, it seems that eating seafood is fraught with danger. Numerous agencies provide guidelines to help us avoid pollutants like PCBs and mercury that accumulate in sea life. On top of that, natural toxins from the marine environment can also be a concern: poisons produced by some types of microorganisms can accumulate in marine life, just as pollutants do. These compounds can cause severe and sometimes fatal illnesses such as paralytic shellfish poisoning and norovirus.

One of the most common illnesses associated with eating seafood is ciguatera fish poisoning. While ciguatera is rarely fatal, it is incurable and has unpleasant symptoms that can last for days, week, or in some rare cases, years. These include nausea, headaches, and neurological symptoms such as numbness and hot/cold reversal (hot things feel icy cold, and cold things feel scorching hot!). Cooking does not lessen the risk of ciguatera, and it’s difficult to test for ciguatera-causing toxins (ciguatoxins) before consumption.

Gambierdiscus toxicus, the toxin-toting microorganism responsible for ciguatera poisioning (Source: http://www.livingoceansfoundation.org/)

Gambierdiscus toxicus, the toxin-toting microorganism responsible for ciguatera poisioning (Source: http://www.livingoceansfoundation.org/)

What Causes Ciguatera Poisoning?

Ciguatoxins are produced by certain species of dinoflagellates (microscopic marine organisms) from the genus Gambierdiscus. These organisms live in benthic (seafloor) environments in equatorial regions. They are often found adhered to plants like algae and seaweed that would be attractive food for herbivorous and omnivorous fish.

Biotransformation and Bioaccumulation

When a fish ingests plant matter that contains Gambierdiscus, toxins from the microscopic organisms are stored in the fish’s body. Like persistent organic pollutants, these toxins are not easily excreted from the body, so they can accumulate over time as the fish continues to eat plants that contain Gambierdiscus. While accumulating in the body, these compounds can also undergo biotransformation, meaning that they are modified by biological processes. Transformed compounds are often similar in chemical structure, but can have strikingly different biological effects. 

We all know what happens next: big fish eats little fish. When large, carnivorous fish prey on small, herbivorous fish contaminated with ciguatoxins, these compounds travel up the food chain, bioaccumulating and biomagnifying in top predators. For this reason, the fish considered most likely to contain dangerously high levels of ciguatoxins are large, predatory reef fish like moray eels, groupers, and barracudas. Since the largest of these fish have lived the longest, it’s likely they will have accumulated even higher concentrations than smaller fish of the same species.

To minimize the risk of ciguatera, many countries have instated guidelines identifying high-risk fish, usually focusing on fish trophic level and size. However, our ability to actually predict which reef fish are safe and which are risky is rudimentary at best. It’s much more complicated than “big fish eats little fish”: food web dynamics in diverse reef ecosystems are poorly understood and highly variable depending on the specific region considered.

Many previous studies on ciguatera focused on the disease’s effects, measuring the toxicity of reef fish from at-risk regions. In this study, researchers focused on the causes of ciguatera by directly measuring levels of three specific ciguatoxins in fish and invertebrates of different trophic levels to determine which fish were most risky to consume and how ciguatoxins move through the reef ecosystem.

Methods

An island in the Republic of Kiribati

An island in the Republic of Kiribati

Researchers traveled to the Republic of Kiribati, a group of islands in the central Pacific Ocean where occurrences of ciguatera have frequently been reported. They identified two locations with a high abundance of Gambierdiscus, the toxin-toting microorganism, where toxicity due to ciguatoxins had previously been reported.

Blue-spotted grouper, known to carry ciguatoxins

Blue-spotted grouper, known to carry ciguatoxins

 

 

 

 

The study focused mainly on the species of greatest concern – blue-spotted grouper, yellow-edged moray, and the giant moray – all large, top predator species. They also measured ciguatoxins in benthic crustaceans and herbivorous and omnivorous fish, aiming to analyze how concentrations of different ciguatoxins change with trophic level (an animal’s position in the food chain) and identify the species that are most effective at transferring toxins to top predators.

The researchers focused on three ciguatoxins called P-CTX-1, P-CTX-2, and PCTX-3, where P-CTX stands for Pacific ciguatoxin. These compounds are not the toxins initially present in dinoflagellates. Rather, they are biotransformation products that form once the toxins have been ingested by fish. Both PCTX-2 and PCT-3 are intermediate compounds that biotransform to become PCTX-1 within fish. PCTX-1, the most potent toxin of the three, does not transform any further. Scientists used an extremely sensitive analytical technique called liquid chromatography-tandem mass spectrometry (LC/MS/MS) to separate out and measure these three toxins in reef fish.

Ciguatoxins analyzed in this study

Ciguatoxins analyzed in this study

To trace the complex reef food web and determine who is eating who, researchers used a technique called nitrogen stable isotope analysis, in which they measure the amount of 15N relative to 14N in each fish species. 15N is generally known to transfer more efficiently from prey to predator, so that fish at higher trophic levels will have higher levels of 15N relative to 14N. While the method isn’t flawless (some organisms scavenge, throwing off stable isotope readings, and there are other parameters that could affect 15N levels besides just trophic level) it provides some guidance when dealing with immensely complex marine food webs.

Results

In a few instances, researchers found different levels of toxins in organisms of similar trophic levels. For example, they found very low levels of P-CTX-1 in octopus and lobster, but they found no trace of any of the toxins in crab. All of these species eat at a similar level on the food chain, but they have different preferences: lobsters and octopuses are expected eat more crustaceans, while crabs may eat more clams and oysters.

Similarly, plant-eating fish that seemed to be of similar trophic level had different levels of the toxins. This data led the researchers to believe that understanding food choice – the specific type of plant a fish species prefers – is crucial in understanding how ciguatoxins transfer to upper trophic levels.

Concentrations of the three toxins measured, and their sum, in a range of species from the complex reef food web.

Concentrations of the three toxins measured, and their sum, in a range of species from the complex reef food web.

As expected, concentrations of ciguatoxins were generally higher in piscivorous (fish-eating) predators. Stable nitrogen analysis confirmed what researchers suspected: groupers and morays seemed to be top predators in the reef ecosystem, and concentrations of the toxins were generally highest in these species, even compared to other predators. Researchers compared trophic level to toxin concentration to determine whether they could observe biomagnification. They found that concentrations of P-CTX-1, the final biotransformation product, did indeed seem to increase from the lowest to highest trophic level, confirming that the toxin biomagnifies. The other intermediate products did not show evidence of biomagnification.

Next, the researchers set out to determine whether the biggest fish were really the most toxic. They found ciguatoxin concentration correlated well with giant moray length and weight: bigger, longer morays were more risky to consume. However, the relationship was not so straightforward in yellow-edged morays or blue groupers. Size and length of these fish did not effectively predict toxin levels. This may be due to complexities of the food web dealing with food choice, etc., that aren’t necessarily detected via stable nitrogen analysis.

Significance

Endangered Hawaiian monk seal, a top predator that could feed on tainted reef fish

Endangered Hawaiian monk seal, a top predator that could feed on tainted reef fish

Diseases like ciguatera poisoning post a risk not only to humans, but also to marine mammals like Hawaiian monk seals that prey on reef fish, many of which are endangered. A better ability to predict risk of ciguatera is crucial in regions like the Republic of Kiribati, where reef fishing provides food for local people and is an important aspect of the economy. Fish are often exported to many other nations, making ciguatera poisoning a global concern.

While this study confirmed what was already understood about ciguatoxins (they tend to be higher in top predators) it also highlighted many of the subtle complexities prevalent in this type of research: food web research is rarely clear-cut and researchers reported some unsuspected findings.

This study highlights how much more there is to learn about what makes a fish too toxic to eat. The simplified view is that “big fish eats little fish,” but real food chains are actually interconnected webs where different species have different dietary preferences and accumulation of hazardous substances can be difficult to trace. This research offers cautionary evidence avoiding larger fish is not a foolproof way to ensure safe seafood.

I am the founder and editor-in-chief of oceanbites, and a 5th year doctoral candidate in the Lohmann Lab at the University of Rhode Island Graduate School of Oceanography. My research focuses on how toxic chemicals like flame retardants end up in our lakes and oceans. Before graduate school, I earned a B.Sc. in chemistry from MIT and spent two years in environmental consulting. When I’m not doing chemistry in the lab, I’m doing chemistry at home (brewing beer).

Discussion

4 Responses to “Big Fish Eats Little Fish: Biomagnification of Natural Toxins”

  1. Hi Carrie, I am interested in your thoughts on ciguatoxins travelling into the human food chain via fish based fertilisers and fish meal in chicken feed. I have a potential client (I am a horticulturalist)who is extremely sensitive to this toxin in her food and so would like my help in growing fruit and vegetables. If you could point me in the right direction for information I would be extremely grateful. Thank you , Libby
    Ps is Tiny an Australian sugar glider?

    Posted by Libby | June 9, 2014, 2:15 am
    • Hi Libby,

      Yes – Tiny is a 7 year old Australian sugar glider!

      I know that there are anecdotal accounts that eating things like chicken and pork can exacerbate symptoms or cause relapses _after_ someone has been exposed to ciguatoxins. However, I haven’t heard of any accounts of the toxin bioaccumulating in meats other than tropical reef fish. Unfortunately, there is a lot we don’t know about ciguatera – its levels in many species of fish and shellfish have never been measured. My feeling would be that the types of fish that are likely to accumulate toxic levels of ciguatoxins are larger predatory fish that aren’t usually primary components of products like fish meal, but I can’t say with 100% certainty. If you are careful to avoid fish and shellfish from regions where the toxin is found (or fish and shellfish of unknown origins) you should be pretty successful at avoiding it.

      There’s a very, very detailed review of ciguatera here: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2579736/

      Hope this helps,
      Carrie

      Posted by Carrie McDonough | June 10, 2014, 3:08 pm

Trackbacks/Pingbacks

  1. […] Another kind of nuisance algae are the species that cause harmful algal blooms, which have adverse effects for both people (e.g. shellfish poisoning) and fish (e.g. mass mortality events). Many experiments on harmful algae species revealed that they grow faster and sometimes produce more toxins under higher temperatures and higher CO2 conditions. With temperature increases happening alongside ocean acidification, this finding is a cause for concern and could inspire many shellfish lovers to lower their carbon footprints. (For more info on shellfish poisoning, read this great oceanbites article!) […]

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