P. oceanica litter: a dynamic food reserve

P. oceanica (Posidonia oceanica) is a flowering plant that lives in abundant meadows covering the seabed along the Mediterranean coast. Its considerable influence on Mediterranean coastal ecosystems is well known, and is being studied by several researchers of the University of Liège from it’s oceanographic research station (STARESO) in Calvi, Corsica. During the four years that François Remy spent working on his PhD thesis(1) at ULg’s oceanology laboratory, he spent nearly one year on STARESO where he explored – both by diving and conducting laboratory analyses – an aspect of these meadows that has not yet been studied much: the role of their litter as a habitat and a food reserve for the communities of invertebrates that inhabit it. This study is unprecedented in scale.

‘P. oceanica meadows are characterised by a very high annual primary production, comparable to that of certain tropical forests. As is the case in forests, P. oceanica leaves – whose average length is around 75 cm – wither and fall off in the Autumn, then grow back again in the Spring,’ explains François Remy. ‘Another particularity of this plant is that its leaves, which are both dense and in high numbers, fall off when they are still mostly untouched by the local herbivore organisms. These dead leaves, or macrophytodetritus, then become stuck in the meadow and decompose there, creating what is known as a litter. The litter sometimes remains inside the meadow, and is sometimes massively pushed out by waves towards unvegetated areas – often sand patches – where it accumulates. These are called exported litters.’ It is no coincidence that P. oceanica leaves are hardly ever consumed live: they contain toxic and repellent compounds that prevent them from being eaten by herbivores and make them edible only to some species of fish and urchin. ‘However, when the leaves fall off, the toxic compounds are released from the dead cells and dissolve in the water. As a result, they are not present in dead P. oceanica leaves.’

While the dead leaves can then be assimilated, they have lost many of the nutrients they once contained, either because they also dissolved in the water or because the plant reabsorbed them just before shedding each leaf (in a process known as remobilisation). ‘This is similar to how trees retrieve nutrients from their leaves before the Autumn, in order not to waste what they have spent so much time producing.’ So these accumulations of dead P. oceanica leaves are not toxic, yet largely also non-nutritious; still, they are sought after by many detritivore micro-organisms: fungi, bacteria, and microalgae immediately start degrading the leaves and take advantage of what few nutrients are still present. These microorganisms are then consumed by a series of invertebrates who, while they did not have to digest dead P. oceanica leaves themselves, directly benefit from them as they consume the microorganisms that digested the leaves. P. oceanica litter is therefore a much more significant ‘detrital compartment’ than it seems, and not just a habitat. ‘They are not just dead leaves.’François Remy even speculates that this organic matter and the detritivores that consume it allow foliar organic matter produced by P. oceanica to be transferred to all food chains on the Mediterranean coast.

A monopoly for Gammarella

‘The goal of my doctoral research was to make the first comprehensive description of the community of mobile invertebrates living in the litter exported from Calvi Bay, and to determine to what extent this P. oceanica litter is a source of food for these invertebrates. Which invertebrates feed off them, and at what time of the year? What variations occur from one season to the next, and from one year to the next? Then, what other invertebrates in higher trophic levels consume these primary consumers and, through them, also indirectly consume dead P. oceanica leaves? In other words, I attempted to offer the first description of the trophic network within which the litter’s organic matter circulates.’ So every year from 2010 to 2012, during each season, François Remy carried out several sampling campaigns at two spots of Calvi Bay in order to gain detailed insight into the organisms that live there as well as their seasonal dynamics. Various types of sieve were used during the 9 diving campaigns in order to separate the target macrofauna (larger than 500 µm) from the accumulated leaves. At the same time, water samples were collected throughout this period both inside and outside the litter; their analysis in the lab would reveal their concentrations in nutrients and oxygen. From the Autumn of 2012 until the Autumn of 2014, other samples were collected on a weekly basis with a view to better understanding not the inter-seasonal or inter-annual variations, but rather the short-term random variations of the fauna living in the meadow’s litter, especially when a storm occurs. The scale of François Remy's work was unprecedented both in terms of duration and comprehensiveness, and it completes the individual studies that had already been carried out on this topic. After over 230 days of fieldwork, François Remy’s research activities had identified some 115 species of invertebrates, far more than the 45 to 80 species that had been inventoried in the literature up until that point. ‘This number seems high, but we should point out that it is three times lower than the total number of species living in the P. oceanica meadow. The litter is therefore not a very diverse environment, but it does host a large number of invertebrates, who are almost twice as abundant as in the meadow.’ Out of the 115 species identified, 77% are arthropods (among which, to the researcher’s surprise, one species is predominant: Gammarella fucicola, a small crustacean), with annelids (12%) and molluscs (7%) trailing far behind.

Oxygen, an important factor among others

‘One observation that stands out is that only 19 species make up 90% of this abundance of organisms,’ which means that the accumulated dead leaves are home to a few organisms that are entirely adapted to a rather inhospitable environment. Food is abundant, but, as we have mentioned, difficult to assimilate. More importantly, the conditions existing inside the litter have proven to be highly variable, requiring constant adaptations from the macrofauna living there. ‘At a depth of only ten metres, the litter is influenced by the movement of the waves: even in the smallest storm, the litter is tossed around by the current and sees its oxygen level rise and fall quickly, sometimes almost to the point of anoxia – the absence of oxygen –, in only a few hours.’ An experiment conducted in October, 2014, demonstrates that the existence of layers with different oxygen concentrations has a direct impact on invertebrates: some species are only present in the litter’s upper layers, where oxygen concentration is higher than in the layers that are closer to the sediments. Conversely, small crustaceans such as Nebalia strausi are present only in the layers of the litter that have low oxygen concentration: this keeps them away from predators and competition, and they seem to tolerate the lower oxygen concentration very well. As for the species that dominates the P. oceanica litter, Gammarella fucicola, it does not appear to be influenced by these changes, as it can be found in all layers of the litter. ‘The influence of oxygen concentration should be put into perspective,’ urges François Remy. ‘My research suggests that the variations only affect a dozen species out of the 115 that have been identified. The vast majority of species are not affected. Generally speaking, the presence or absence of certain species at certain times of the year is related to other factors, which were not studied here.’

The same is true, explains the researcher, of seasonal variations: it is hardly surprising that litter is more abundant in the Autumn and in the Winter, i.e. when P. oceanica sheds its leaves, than in the Spring and in the Summer. However, while these seasonal variations do have an influence on the number of invertebrates living in the litter, have virtually no effect on their diversity. There is another type of phenomenon observed in the P. oceanica litter that is much more random, intense, and limited in time: ‘resource pulses’. Resource pulses occur during storms and gusts of wind, and can have a significant structuring role on the invertebrates living in the litter. When strong currents stir up the litter deposits and remove dead leaves (up to 99% of the litter), some organisms follow these dead leaves or migrate to a different environment and might eventually return at a later point. Others, however, are strongly attached to the litter and choose to remain in the few remaining accumulations. ‘In other words, they would rather remain in a harsher environment with a higher density of organisms and, therefore, more competition. This is probably because they would be unable to survive optimally in other environments.’ Such is the case of amphipod Gammarella fucicola: this small crustacean is present, as mentioned previously, in layers of the litter that have both high and low oxygen concentrations, and it is among the organisms that, when many dead leaves are removed, prefer to stay in what is left of the litter. ‘A number of hypotheses can be suggested to explain this: this species may have lower chances of survival in other environments and would not entirely belong, for instance, in the meadow itself, only a few metres from the accumulated dead leaves – it is not found in the meadow itself, but only in its litter –, or it may be more advantageous for Gammarella fucicola to temporarily live with increased competition with other gammarellidae or with otheramphipods, as dead leaves always eventually return, rather than spend considerable energy migrating to another environment. In any case, Gammarella fucicola seems to be remarkably well adapted to living in the litter.’

Looking at stomachs under the microscope

An inventory of the community of invertebrates living in the litter should, according to François Remy, immediately be followed by an analysis of their diets. Could a study of these diets corroborate the hypothesis that litter-consuming invertebrates are responsible for transferring the energy stored during P. oceanica’s leaf production to all coastal food chains in the Mediterranean? After all, P. oceanica litter is not limited to dead leaves: it also includes over potential food sources such as algae, but also epiphytes (bryozoans, hydrozoans, bacteria, fungi, microalgae, etc.) that grow on the surface of P. oceanica leaves. So François Remy spent months analysing the stomach content of some 560 microorganisms and, by comparing the results with analyses of stable isotopes of carbon, nitrogen and sulphur, attempted to determine the general diet of 19 species out of the 115 that were identified initially. This allowed him to observe, in addition to unexpected content such as textile fibre (read Microplastics in fish stomachs), the existence of trophic levels, that is to say several levels within a single trophic network (a series of food chains): primary consumers such as Gammarella fucicola, omnivores such as Nebalia strausi, carnivores such as Liocarcinus navigator, a small crab, or Palaemon xiphias, a shrimp, and even possible top predators who prey on carnivores, such as young fish in the Gobius genus. However, each of these trophic levels seems to have its own dietary preferences: some primary consumers such as G. fucicola are mixed consumers – they ingest a combination of algae, epiphytes, and dead leaves – while others have more of a detritivore diet, eating essentially dead leaves (e.g. Gammarus aequicauda, 60% of whose diet is dead leaves). ‘Since predators consume these invertebrates, and since top predators then eat those predators, it is easy to understand how the organic matter from dead leaves is transferred from the litter to top predators through these “litter consumers”. Litter therefore appears to be a non-negligible source of food for all coastal ecosystems in the Mediterranean, even though P. oceanica meadows contain other sources of food that can be assimilated more easily.’

(1) Characterization, dynamics and trophic ecology of macrofauna associated to seagrass macrophytodetritus accumulations (Calvi Bay, Mediterranean Sea), Thèse de Doctorat 2016

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(1) Characterization, dynamics and trophic ecology of macrofauna associated to seagrass macrophytodetritus accumulations (Calvi Bay, Mediterranean Sea), Thèse de Doctorat 2016