Domoic acid contamination within eight representative species from the benthic food web of Monterey Bay, California, USA

Phytoplankton are at the base of many food webs, hence if these produce toxins that are harmful to organisms at higher trophic levels, and these toxins can be passed up via the food chain, they will have major implications for the health of those organisms. Domoic acid has been named as a toxin produced by phytoplankton that causes disorientation, memory loss, seizures, coma and death. It is possible for organisms to contain low levels of DA without exhibiting these effects. This allows for low levels in prey to be passed up to organisms through the food chain, resulting in higher concentrations at higher trophic levels. This process is understood in pelagic food webs but not benthic food webs. Kvitek1 et al (2008) investigated the levels of DA in organisms at different trophic levels of a benthic food web, using Pseudonitschia species as reference due to their common occurrence in the sampling area, and ability to produce DA.

Samples of organisms, and seawater from the top, middle, and bottom, were collected from Del Monte Beach in the southern bight of Monterey Bay, California. Eight benthic species, Urechis caupo, Emerita analoga, Nassarius fossatus, Citharichthys sordidus, Neotrypaea californiensis, Pagurus samuelis, Dendraster excentricus and Olivella biplicata, were chosen as they represent several different trophic levels, feeding styles and a link to higher organisms such as sea birds. Collection occurred 3 times a week in Pseudo-nitzschia australis bloom conditions and every 2 weeks when a bloom was lacking. Sampling spanned 2 distinct blooming events and one small bloom, from autumn 2000 to autumn 2001.

 

Pseudo-nitzschia species were identified by incubating small aliquots of water with fluorescently P. australis and P. multiseries (the local species) species-specific probes, then observed under a compound microscope and florescent light, from which volume-specific abundances were calculated. The concentration of DA was determined using high-performance liquid chromatography (HPLC) on filtered water column samples and extracts of homogenised animals. Emerita analoga was analysed used a reverse phase of HPLC. Several small organisms were homogenised from the same species to create equal volumes across all species. The efficiency of this method was tested by injected known amounts of DA standard into tissue of Urechis caupo and Dendraster excentricus, which had not been tested in previous research, and following the method of this experiment.Further investigation occurred into Urechis caupo due to no previous research confirming the presence of DA in their phylum, Echiura, despite DA detection for all samples during this experiment. Isolation of the peak fractions and selective ion monitoring of mass spectrometry data, then assays, confirmed the identity of DA and toxicity, respectively.

Statistical analysis occurred using Pearson correlation and paired t-tests to compare: water column DA concentrations and cell density of Pseudonitschia; water depth and water column DA concentration; and DA tissue concentrations during blooms and when a bloom was lacking. Additionally, linear regression was used to determine strength of the relationship between water column DA concentrations and cell density of Pseudonitschia.

The abundance of P. australis and P. multiseries peaked during blooms in autumn 2000, and spring and autumn 2001. Overall, the strength of the relationship between water column DA concentrations and cell density of Pseudonitschia was weak. Kvitek1 et al (2008) presumed that the DA was produced by pseudo-nitzschia species, however it is possible for other sources to produce these, such as other diatoms. It seems likely due to the independence of DA concentrations and P. australis and P. multiseries densities.  

The relationship between toxin levels and that of the water column, and toxin retention levels, varies between organisms of different trophic levels. If the hypothesis stated for the pelagic food web was also true for the benthic food web, an increase in toxin levels would be observed the higher the food web. However this is not the case. The average DA concentrations of the organisms during blooms were the highest for 2 filter-feeding species; moderate levels for the 2 scavengers, a predator, and a deposit-feeding shrimp; lowest levels for the remaining 2 deposit-feeders, with 1 also having the second feeding method of filter feeding. Logically speaking, the filter feeders should have high levels considering their direct ingestion of the Pseudonitschia species and toxins. The concentration appears to reduce further up the food chain, which could be a result of higher organisms feeding on other species that do not accumulate DA that have not been investigated in this study.

 

There was a low extraction efficiency noted for Dendraster excentricus, hence it might have been falsely identified as having lower levels than the other 2 filter feeders. On the same note, the efficiencies for the other species were not checked. Considering the validity of this method was shown as questionable, surely Kvitek1 et al (2008) would have checked.  They also state that 5 species contained significantly higher concentrations of DA during the blooms, and 3 species appear to retain the toxin momentarily after a bloom. This may not be retention but evidence that there is another source of DA in the environment.

 

They stated that DA was distributed evenly over all depths, therefore used the values of DA at the surface in comparisons between water content and animal content. When I looked at the data there did seem to be a peak of DA at 7m approximately twice the DA concentration of the surface and 25m. The species investigated inhabit different depths, and considering the variation in DA they should have compared the DA levels in the water at the same depth as the organism.

No comments were made on the health of the organisms when they were collected, and some collection techniques even involved killing the organism whilst in the water still. Considering DA is a neurotoxin and can cause behavioural changes, surely the behaviour of the animal should have been investigated even in brief to see if the levels present where effecting them.  

They also did not comment on the abundance of the animals present, neither those investigated or others, and the number of species considered is small. The weakness of the relationship could be due to the presence of organisms that interact with DA in some way. For example: uptake DA from the environment or alter the levels via some form of external detoxification system. 6 species exceeded levels of DA thought to be safe for higher level consumers. They could compare their findings to data collected on the abundance of higher trophic level organisms known to feed to these, or consider any reported mortalities that occurred at the time.

This study highlights the ability of domoic acid to manifest in these marine organisms of varying feeding styles and trophic levels, still within low levels overall. It suggests the transfer of the toxin is different in the benthic food web than in the pelagic food web in that concentrations of DA do not increase further up the trophic levels. However several more studies using different organisms, and considering different sources of the toxin, would be necessary to confirm the findings. The extraction method may also need changing as the one used is not efficient for all species. There is potential for cross-referencing to occur of this data with other data collected at the same time about other organisms inhabiting the area, and environmental changes. Due to the complexity of the food web this would be largely beneficial, although time consuming and impossible to do for all species.

Kvitek1, R. G; Goldberg, J. D; Smith, G. J; Doucette, G. J; Silver, M. W (2008) Domoic acid contamination within eight representative species from the benthic food web of Monterey Bay, California, USA, MARINE ECOLOGY PROGRESS SERIES, 367: 35–47