by Matthew Cobb
[Jerry’s poorly at the moment, so he’s invited his guest bloggers to pitch in. Get well soon, Coyne!]
This fantastic picture is of a Hyperiid amphipod – a small (1.5 cm) shrimpy thing, but most definitely not a shrimp. It is one a set of photos that has been going the rounds in the media, following a recent series of publications by the Census of Marine Life – an international network of marine scientists. This set of 16 beasties appeared in The Guardian.
The CoML folk estimate there are around marine 230,000 species (seems pretty low to me), and describe their findings in a series of articles in the PLoS ONE open access journal. These include one with the great title “Deep-sea biodiversity in the Mediterranean Sea: The known, the unknown, and the unknowable”. All highly recommended.
But back to the amphipod. But what caught my attention was the caption given to it by The Guardian: “Pelagic amphipod, Phronima sedentaria. It travels in a ‘house’ that is a cylindrical-shaped organism whose body has an opening on both ends. Gulf of Mexico.”
Apart from hoping that P. sedentaria and its pals live way away from the Deepwater Horizon spill, I was intrigued by the “house”: what kind of organism is it, and why on earth would it accept having a shrimp-that-isn’t-a-shrimp living inside it?
The answer to the first question is remarkable. The “house” is a thing called a salp, and its an animal. Looking at it, you might think it was something like a jellyfish, but not at all. It has a well-organised nervous system and is in fact a chordate, just like you and me and my cats. More specifically, it’s a tunicate, like a sea squirt.
This diagram from the Tasmanian Aquaculture and Fisheries Institute, shows the salp’s structure – it has a series of circular muscles going round the body, a mouth, an anus, and a through gut. It moves – and eats – by ingesting water and squirting it out through its rear end. As well as being a neat trick requiring neuronal coordination, these fecal pellets form an important part of the marine ecoystem. As K. Iseki wrote in 1981:
“Free-floating sediment traps were suspended at 200 and 900 m in the northern North Pacific Ocean during 20-21 May, 1974. A considerable amount of large, dark-green particles, larger than 1 mm in diameter, was collected at both depths. These large particles corresponded morphologically with fecal pellets of salps. Vertical carbon flux was estimated to be 10.5 and 6.7 mg C m-2 d-1 at 200 and 900 m, respectively. This suggests that vertical transport of salp fecal pellets could play an important role in meeting the energy requirements of bathypelagic organisms in the open ocean.”
Salp are a particularly important of the zooplankton, and together with the more widely-known krill, they consume vast quantities of phytoplankton. Due to increases in salp numbers in the Southern Ocean, apparently due to global warming, the krill may be being replaced by salp within the Antarctic marine ecoystem. This in turn might have unknown consequences on larger, more photogenic marine animals.
The excellent jellieszone.com has this summary of the complicated salp life-cycle (wake up at the back, there will be a quiz later on):
“Salps can form massive aggregations of millions of individuals that may play a significant role in marine ecosystems. They exhibit among the fastest growth rates of any multicellular organism. (…) Salps exhibit a complex life cycle with alternating aggregate and solitary generations. Aggregates (the sexual gonozooids) develop asexually from an elongating stolon that buds from an area just behind the endostyle of the solitary individuals (the oozooid). Individuals within aggregates are hermaphrodites, typically starting as females that are fertilized by older male individuals from another chain. The resulting embryos (oozooids) then develop into the solitary asexual phase. There is no larval stage and even before release the young oozooid often has a developing stolon. In many species only a single embryo develops within each individual of the aggregate. This method of asexual reproduction enables salps to quickly exploit periods of abundant food with rapid increases in population density.”
The article concludes where we began:
“Hyperiid amphipods and several species of fish also use salps as traveling homes.”
Now from the amphipod’s point of view the relationship with the salp seems quite understandable – it could serve as some kind of protection against predators, or maybe save them energy.
But what does the salp get from transporting P. sedentaria up and down the water column? The answer appears to be: nothing. As the webpage of Sönke Johnsen’s lab at Duke University puts it, the “house” is nothing more than “a hollowed-out salp test” (the test is the salp’s “shell”). This suggests to me that the salp has died or discarded the test, and the amphipod simply takes up residence, like a hermit crab.
Things are in fact more complicated, more fascinating and more gruesome.
In 1978 Philippe Laval from Villefranche in France, measured 70 “houses” fished up from the sea off Nice and subjected his findings to some complicated statistical analysis. He found that the houses broke down into five groups and belonged to either salps or pyrosomes (another form of tunicate that can bioluminesce).
Amazingly, it seems that the “house” is actually sculpted by the amphipod:
“It was shown that all the tissues were carefully removed by the amphipod (in salps as in pyrosomes), leaving only the tunic. (…) The inner surface is generally scraped off, perhaps to eliminate decomposing secondary ascidiozooids remaining in the test after zooid extraction. The inner surface is extremely smooth, as though finished with a fine cutting tool on a lathe. This could explain, besides the high variability, why principal component analysis did not disclose distinct groups of barrels. The inside is always made hollower in the middle, so that the wall is thicker at both ends. Less rigidity in the middle could produce the swelling leading to the barrel-like shape, but there could be also a mechanical distention by the rotating amphipod before tunic consolidation.”
On reading this, I assumed the tunicate had been eaten before all this sculpting and scraping went on. Not at all. Laval concludes, with words that suggest the relationship with the Alien is not merely morphological:
“Finally, the relationship between Phronima and its barrel deserves some consideration. It is not in essence predaceous, because salps or pyrosomes are not primrily used as food (although they may be, besides making a barrel); moreover, the amphipod remains with – within – its partner. It is rather a borderline case of parasitism, soon fatal to the host, which is killed to obtain advantages from its tunic. Some hermit crabs are known which similarly kill and eat molluscs before occupying the shells (Rutherford, 1977). Most of the hyperiid amphipods (if not all, as postulated by Harbison et al., 1977) are parasitic on pelagic animals. Phronimids, which deposit their larvae in the barrel, as do many hyperiids on their hosts (Laval, 1965), are not exceptions to the rule. By killing their host and removing its soft parts to prevent decay, they only go a step further and thus approach the margins of predation.”
To complete the story, in 2005 Euichi Hirose and co-workers studied seven “houses” and suggested they were indeed still alive – cells were still alive and there were no bacteria in the barrels, suggesting there was some kind of antibiotic system in there. And Renée Bishop & Stephen Geiger looked at the energetics of being a Phronima compared to other crustaceans and concluded:
“Although less energy is needed to remain in the water column since the gelatinous zooplankton makes the Phronima more buoyant than just Phronima alone, metabolicrates of Phronima are not lower than those of other pelagic crustaceans, possibly due to the energy needed to propel the barrel. However, Phronima have lower protein concentrations, indicating less energy is allocated to muscle production. The ratio of LDH (L-lactate dehydrogenase) activity to CS (citrate synthase) activity was >1, indicating that burst swimming is important in Phronima‘s metabolism. The symbiotic relationship provides the Phronima with food and a substrate for the brooding of young, but does not give them an energetic advantage over other pelagic crustaceans.”
So they have a house and food, but they still have to swim!
That’s an awful lot of information to come from one intriguing photo…
Euichi Hirose, Masakazu N. Aok & Jun Nishikawa (2005) Still alive? Fine structure of the barrels made by Phronima (Crustacea: Amphipoda). Journal of the Marine Biological Association of the United Kingdom 85:1435-1439.
E. A. Pakhomov, P. W. Fronemanb & R. Perissinottoc (2002). Salp/krill interactions in the Southern Ocean: spatial segregation and implications for the carbon flux. Deep Sea Research Part II: Topical Studies in Oceanography 49:1881-1907