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Biology

Marine herbivores “steal” and use chemical defenses from algal hosts

 

 

Article: Amsler, M.O, et al. “Tolerance and sequestration of macroalgal chemical defenses by an Antarctic amphipod: a ‘cheater’ among mutualists. Marine Ecology Progress Series (2013) 490: 79-90.

Doi: 10.3354/meps10446

Introduction:

Macroalgae, or seaweed, plays a pivotal role in marine ecosystems. As the base of the food web, these organisms provide energy for the rest of the ecosystem: herbivores consume them and pass energy up the food chain. But like any organism trying to survive, many seaweeds have evolved defense mechanisms. Similar to some land plants, a number of algae contain chemical compounds that deter herbivores and help prevent consumption. But the relationship between marine herbivores and algae is complex. Small herbivores, like amphipods (small marine arthropods), have been shown to exhibit a mutualism with certain species of chemically defended algae. In this relationship, the chemically defended algae provides habitat and refuge from omnivorous predators and in return the amphipods graze and clean the algae of any epiphytic species (or algae that tries to grow on the host) competing for light and nutrients. In this relationship both the herbivore and the algae benefit.

Some terrestrial and marine herbivores have evolved physiological and behavioral methods of dealing with chemically defended plant material, allowing for ingestion. In some rare cases, consumers are able to sequester the plant or algal toxins within their tissues and use them for defense against predation. Sequestration of chemical compounds has only been documented in one marine clade.

The amphipod Paradexamine fissicauda

Fig 1: The amphipod Paradexamine fissicauda

In the Antarctic, coastal ecosystems are dominated by large, complex macroalgae, many of which have chemical defenses. Prior studies have shown that many different amphipod species live in association with these seaweeds and appear in abundance. These studies examined the relationship between herbivore and host to test for true mutualism. Gut contents from just one species of amphipod, Paradexamine fissicauda (Fig 1), showed isotopic traces that could be linked to consumption of one of the most common chemically defended seaweeds in this region, the branched red algae Plocamium cartilagineum (Fig 2). These findings piqued the interest of current researchers at Palmer Station, Antarctica, and a study began looking at whether or not other amphipods could eat this chemically defended algae and if chemical sequestration helps protect amphipods from predation.

The chemically defended seaweed Plocamium cartilagineum.

Fig 2: The chemically defended seaweed Plocamium cartilagineum.

The Study:

Beginning in 2010, researchers at Palmer Station collected 6 species of local amphipods and 8 species of local, palatable (or commonly consumed) macroalgae (some chemically defended, some not). The amphipod Paradexamine fissicauda and the red alga Plocamium cartilagineum were included in the study. Organisms were brought back to the laboratory at the station and acclimated to lab conditions.

In the first phase, researchers fed the 6 amphipod species a diet of only the chemically defended algae Plocamium cartilagineum. Results from this phase (Fig 3) indicated that P. fissicauda was the only amphipod to consume the chemically defended algae at an appreciable rate.

Taking the results from the first phase, researchers began phase two: testing the feeding preferences and feeding rates of P. fisscauda. Feeding rates (in units of weight per hour) of P. fissicauda on 8 species on algae were determined. Researchers used two different feeding trials to test both preference and rate. The first trial was called a “no-choice” trial in which the amphipod was only given one algal species to consume. The second trial was a “choice” trial in which the amphipod was presented with 4 species of algae to choose from to consume. It was found that this amphipod would appreciably consume several species of algae when given “no-choice,” including consumption of P. cartilagineum. But researchers also found that the feeding rate on P. cartilagineum was the highest in choice trials (Fig 4). It seems that either way, P. fissicauda are actively grazing on P. cartilagineum. 

Fig 5: Graph shows the percent of P. fissicauda eaten by fish based on diet. Another similar amphipod is shown on the far right, this was included to rule out shape and structure of amphipods playing a role is being eaten.

Fig 5: Graph shows the percent of P. fissicauda eaten by fish based on diet. Another similar amphipod is shown on the far right, this was included to rule out shape and structure of amphipods playing a role in being eaten.

Fig 3: Graph showing the feeding rates of 6 amphipod species on P. cartilagineum.

Fig 3: Graph showing the feeding rates of 6 amphipod species on P. cartilagineum.

Fig 5: Graph showing the results of the "choice" feeding trial. Shows feeding rates of P. fissicauda on 4 species of algae.

Fig 4: Graph showing the results of the “choice” feeding trial. Shows feeding rates of P. fissicauda on 4 species of algae.

The final piece of this experiment, phase three, was to determine if the sequestration of chemical compounds by P. fissicauda effectively lowered its chances of being eaten. In this phase researchers fed P. fisscauda a diet of P. cartilagineum as well as a diet of a non-chemically defended algae (to act as a control). After a few days of feeding, amphipods were briefly immobilized and placed in front of a fish predator and the percent of amphipods eaten was recorded. It was found that amphipods that were fed the chemically defended algae were consumed less than 20% of the time compared to those on a non-chemical diet; which were consumed greater than 50% of the time (Fig 5).

Significance:

This is only the second documented example of chemical sequestration by a marine organism, and the first by any marine arthropod. Although the processes behind the actual sequestration from algae are unclear, what is clear is that the amphipod P. fissicauda is using the sequestered chemical compounds successfully for it’s own defense against predation. The amphipods and chemically defended algal species in this ecosystem were thought to be in a community-wide mutualism, where the amphipods gained refuge from the algae and the algae were benefitted by the amphipods eating the competing epiphytic algae. As a result of this study, researchers are taking a closer look at these relationships, as it seems that at least one species has been cheating the system, taking more from their algal hosts than they are giving.

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