Arnaud-Haond S, Duarte CM, Diaz-Almela E, Marbà N, Sintes T, et al. (2012) Implications of Extreme Life Span in Clonal Organisms: Millenary Clones in Meadows of the Threatened SeagrassPosidonia oceanica. PLoS ONE 7(2): e30454. doi:10.1371/journal.pone.0030454
Editor:Hans Henrik Bruun, University Copenhagen, Denmark
Abstract The maximum size and age that clonal organisms can reach remains poorly known, although we do know that the largest natural clones can extend over hundreds or thousands of metres and potentially live for centuries. We made a review of findings to date, which reveal that the maximum clone age and size estimates reported in the literature are typically limited by the scale of sampling, and may grossly underestimate the maximum age and size of clonal organisms. A case study presented here shows the occurrence of clones of slow-growing marine angiosperm Posidonia oceanica at spatial scales ranging from metres to hundreds of kilometres, using microsatellites on 1544 sampling units from a total of 40 locations across the Mediterranean Sea. This analysis revealed the presence, with a prevalence of 3.5 to 8.9%, of very large clones spreading over one to several (up to 15) kilometres at the different locations. Using estimates from field studies and models of the clonal growth of P. oceanica, we estimated these large clones to be hundreds to thousands of years old, suggesting the evolution of general purpose genotypes with large phenotypic plasticity in this species. These results, obtained combining genetics, demography and model-based calculations, question present knowledge and understanding of the spreading capacity and life span of plant clones. These findings call for further research on these life history traits associated with clonality, considering their possible ecological and evolutionary implications. The maximum size and age that clonal organisms can reach remains poorly known, although we do know that the largest natural clones can extend over hundreds or thousands of metres and potentially live for centuries. We made a review of findings to date, which reveal that the maximum clone age and size estimates reported in the literature are typically limited by the scale of sampling, and may grossly underestimate the maximum age and size of clonal organisms. A case study presented here shows the occurrence of clones of slow-growing marine angiosperm Posidonia oceanica at spatial scales ranging from metres to hundreds of kilometres, using microsatellites on 1544 sampling units from a total of 40 locations across the Mediterranean Sea. This analysis revealed the presence, with a prevalence of 3.5 to 8.9%, of very large clones spreading over one to several (up to 15) kilometres at the different locations. Using estimates from field studies and models of the clonal growth of P. oceanica, we estimated these large clones to be hundreds to thousands of years old, suggesting the evolution of general purpose genotypes with large phenotypic plasticity in this species. These results, obtained combining genetics, demography and model-based calculations, question present knowledge and understanding of the spreading capacity and life span of plant clones. These findings call for further research on these life history traits associated with clonality, considering their possible ecological and evolutionary implications.Posidonia oceanica, commonly known as Neptune Grass or Mediterranean tapeweed, is a marine flowering plant endemic to the Mediterranean Sea. Like other seagrasses, it forms large underwater meadows in the submerged photic zone of sheltered coastal waters (Pirog 2011). Due to its high rate of primary production and its ability to structure and stabilize the seabed, Neptune grass creates habitat for many other marine organisms and thus plays a significant role in littoral Mediterranean ecosystems (Gobert et al. 2006, Kendrick et al. 2005, Pergent et al. 1994).
Posidonia oceanica is one of the largest, slowest growing, and longest-lived plants. In a recent genetic study of 40 P. oceanica populations across the Mediterranean, Arnaud-Haond et al. (2012) found individual clones spanning up to 15 km (9.3 miles). Based on the plant's known growth rate, such individuals are likely to be thousands, possibly tens of thousands of years old (Arnaud-Haond et al. 2012) .
With their origin possibly dating back to the Pleistocene, some P. oceanica meadows have shown great resilience, persisting through great environmental changes over millennia. Yet, today P. oceanica populations are declining rapidly due to human-induced disturbances (Ardizzone et al. 2006, Duarte 2002, Marbà et al. 1996, 2005, Montefalcone et al. 2007, Waycott et al. 2009). Major threats include coastal construction (Badalamenti et al. 2006, Ruiz & Romero 2003), trawling (Gonzalez-Correa et al. 2005), fish farming (Díaz-Almela et al. 2008, Pergent-Martini 2006), and climate change (Marbà & Duarte 1997, 2009). Arnaud-Haond et al. (2012) warn that "the ancient meadows of P. oceanica are declining at a rate several hundred-fold faster (about 5%.yr−1, Marbà et al 2005, Waycott et al. 2009) than the rate over which they spread when forming (Doyle & Doyle 1987, Sintes 2006), a situation that this slow growing, long-lived species is poorly capable of recovering from."
Posidonia oceanica, commonly known as Neptune grass or Mediterranean tapeweed, is a seagrass species that is endemic to the Mediterranean Sea. It forms large underwater meadows that are an important part of the ecosystem. The fruit is free floating and known in Italy as "the olive of the sea" (l'oliva di mare[2]). Balls of fibrous material from its foliage, known as egagropili or Neptune balls,[3] wash up to nearby shorelines.
The Posidonia has a very high carbon absorption capacity, being able to soak up 15 times more carbon dioxide every year than a similar sized piece of the Amazon rainforest.[4]
Posidonia oceanica has roots (which mainly serve to anchor the plant to the substrate), rhizome and tapeform leaves.
The rhizomes, up to 1 cm thick, grow both horizontally (plagiotropic rhizomes), and vertically (orthotropic rhizomes). The former, thanks to the presence at the bottom of lignited roots up to 15 cm long, anchor the plant to the substrate. The latter, which increase height, have the function of combatting sanding due to continuous sedimentation. The two types of growth give rise to the so-called "kill", a terrace formation that consists of a network of strata of rhizomes, roots and trapped sediments. In this way, posidonias colonise an environment that algae could hardly occupy due to the lack of roots.
The leaves arise from orthotropic rhizomes, are cyntiform and bright green in colour that turns brown over time. They can reach a length of approximately 1.5 metres high. On average they have a width of 1 cm and have 13 to 17 parallel ribs. The apexes are rounded and are often lost by the action of waves and currents.
They are organised in bushes of 6 or 7 leaves, being the oldest on the outside and the youngest on the inside. The leaves are divided into three categories:
Posidonia oceanica reproduces both sexually and asexually (by stolons).
Sexual reproduction occurs through the production of flowers and fruits. The flowers are hermaphrodite and are grouped in a herringbone-shaped inflorescence, green in colour and contained between floral bracts. The peduncle binds to the rhizome in the centre of the bunch. The gynaecium is formed by a unilocular ovary that continues with a style and ends in the stigma. The androecium consists of three stamens with short anthers. Flowering depends on environmental factors (light and temperature) and endogenous factors (age and size of the plant) and takes place in September and October in the meadows closest to the sea surface, while in the deepest ones it is postponed for two months. Pollen inside the anthers is spherical in shape, but becomes filamentous as soon as it is released into the water. There are no recognition mechanisms between pollen and stigma that prevent self-fertilisation. Pollination is hydrophilic and can lead to fruit formation, although some of them do not reach maturation, which occurs after six months. Once ripe, the fruits separate and float on the surface.
The fruit, slightly fleshy and called in some places "sea oiva", is similar to a drupe and has a porous pericarp and rich in an oily substance that allows flotation. When it rots, it releases a seed (coated by a thin membrane, but without a true and proper tegument),5 which falls to the bottom and, if it finds the right conditions of depth, stability and type of sediment, germinates and gives rise to a new plant. In order for it to be consolidated, it is necessary that you find a moisturised substrate. Humidification consists of the degradation of plant remains, so the plant can be implanted in "soils" previously colonised by other plants, such as macroalgae or other phanerogams. Thus, a true ecological succession is generated in which posidonia represents the last stage. Germination begins with the release of a small white root of radical pole and a leaf of the apical pole. With sexual reproduction, the plant colonises new areas, diffuses meadows in other areas and guarantees genetic variability.
Asexual reproduction by stolons, which allows the expansion of meadows, is carried out through plagiargiotropic rhizomes, which grow about 7 cm a year and colonise new spaces. The high accumulation of sediments and the reduction of the space available for horizontal growth stimulates the vertical growth of the rhizomes, thus forming the bushes.
The genus Posidonia is named after Poseidon, the Greek god of the seas, while oceanica refers to its former wide distribution. Carl Linnaeus gave the first botanical description of this species in Systema Naturae, although the genus was then named Zostera. The APG system (1998) and APG II system (2003) accept the genus as constituting the sole genus in the family Posidoniaceae, which it places in the order Alismatales, in the clade monocots. The Angiosperm Phylogeny Website concludes that the three families Cymodoceaceae, Posidoniaceae and Ruppiaceae form a monophyletic group.[5] Earlier systems classified this genus in the family Potamogetonaceae or in the family Posidoniaceae but belonging to order Zosterales. It was published in: A. R. Delile, Description de l'Égypte, in 1813.[6]
Posidonia oceanica is a flowering plant which lives in dense meadows or along channels in the sands of the Mediterranean. It is found at depths from 1–35 metres (3.3–114.8 ft),[7] depending on the water clarity. Subsurface rhizomes and roots stabilize the plant while erect rhizomes and leaves reduce silt accumulation.
The leaves are ribbon-like, appearing in tufts of 6 or 7, and up to 1.5 metres (4.9 ft) long. Average leaf width is around 10 millimetres (0.39 in). The leaves are bright green, perhaps turning brown with age, and have 13 to 17 parallel veins. The leaf terminus is rounded or sometimes absent because of damage. Leaves are arranged in groups, with older leaves on the outside, longer and differing in form from the younger leaves they surround.
The rhizome type stems are found in two forms: one growing up to 150 centimetres (59 in) beneath the sand and the other rising above the sand. All stems are approximately 10 millimetres (0.39 in) thick and upright in habit. This arrangement of the rhizomes eventually forms a mat; the surface contains the active parts of the plant, whereas the center is a dense network of roots and decomposing stems.
The flowering plant's common name is Neptune grass.[8]
In 2006 a huge clonal colony of P. oceanica was discovered south of the island of Ibiza and stretches as far south as La Savina and Es Pujols on the island of Formentera. At 8 kilometres (5.0 mi) across, and estimated at 100,000 years old,[9] it may be one of the largest and oldest clonal colonies on Earth.[10][11][12]
Dead rhizomes with olive-mill waste are used for compost.[13]
This species is found only in the Mediterranean Sea, where it is in decline, occupying an area of about 3% of the basin. This corresponds to a surface area of about 38,000 square kilometres (15,000 sq mi). Posidonia grows best in clean waters, and its presence is a marker for lack of pollution.[14] The presence of Posidonia can be detected by the masses of decomposing leaves on beaches. Such plant material has been used for composting, but Italian laws prohibit the use of marine algae and plants for this purpose.[15]
The UNESCO World Heritage Site around the Balearic Islands of Mallorca and Formentera includes about 55,000 hectares (140,000 acres) of Posidonia oceanica, which has global significance because of the amount of carbon dioxide it absorbs, given the effect of carbon dioxide on climate change. However, the meadows are being threatened by rising temperatures, which slows down its growth, as well as damage from anchors.[16]
The characteristics of the Posidonia plant, its growth dynamics and the large amount of biomass produced, are factors that can sustain very diverse plant and animal communities. Distinguished are: epiphytic communities (that is, bacteria, algae and bryozoa that colonise the surface of the leaves and rhizomes of the plant), vagile and sessile animal communities and communities of detritivorous organisms.
Along the leaf, successions and neighbourhoods that follow the age of the leaf can be identified. Diatoms and bacteria are implanted near the base of the leaf and on the young leaves. Subsequently, in the central part, red and brown fouling algae are implanted, while above the incrustants and in the apical area live erect filamentous algae.
Epiphytic communities are consumed by gastropod molluscs, amphipod crustaceans and polychaetes, and play a very important role in the food chain of Posidonia meadows, taking into account the fact that few organisms are able to feed directly from the plant tissue, little appetising for herbivores due to the high percentage Epiphytes, however, can also damage the plant. In fact, by increasing weight, they can cause premature fall of the leaves, decrease light and also hinder gas exchanges and the absorption of nutrients through the leaves.
Posidonia has been used for about twenty years as a biological indicator. In fact, the plant has all the characteristics of a good bioindicator:
Isolated matine of Posidonia oceanica. The analysis of the density of the bushes is one of the methods of studying meadows.
Therefore, through the study of meadows it is possible to know quite reliably the environmental quality of coastal marine waters.
Generally, the methods of studying Posidonia meadows are four:
There is a close relationship between the depth of the lower limit and the transparency of water.
As for density, it depends on the depth at which the meadow is located, the luminous intensity and the type of substrate. According to the density of the foliar fascicles, measured in number of bushes / m2, meadows are divided into 5 classes.
Phenological analyses allow to study different useful parameters to describe the state of health of plants:
Lepidochronological analysis consists of the study of the life cycles of P. oceanica leaves, which at the time of their separation, once dead, leave the basal part on the rhizome of the plant. These residues, which over time become splinters, have variable thicknesses with annual cyclical trends, useful for the study of environmental variables. Their objectives can be summarised as follows:
To date 51 natural products have been reported from P. oceanica, including natural phenols, phenylmethane derivatives, phenylethane derivatives, phenylpropane derivatives and their esters, chalkones, flavonols, 5-alpha-cholestanes, and cholest-5-enes. Many of the compounds reported for P. oceanica were, however, not detected by appropriate phytochemical methods and some most probably represent artifacts and are not genuine natural products of P. oceanica.[17]
Posidonia oceanica has similar characteristics to terrestrial plants, such as roots, rhizomatous stem and cintiform leaves up to one metre long arranged in clumps of 6 to 7. It flowers in autumn and produces floating fruits in spring, commonly known as sea olives.
It forms underwater meadows of considerable ecological importance. It constitutes the climax community of the Mediterranean Sea and plays an important role in protecting the coastline from erosion. It is home to many animal and plant organisms that find food and protection in the meadows. It is considered a good.
- They fix CO2 and produce oxygen.
- They protect the sandy coastline against erosion.
- They are a reserve of biodiversity due to the large number of animal and plant species that find within the habitat a place for feeding, protection and nursery for juveniles.
- They produce a large part of the sediment that forms part of the sand on our beaches.
Posidonia oceanica, commonly known as Neptune grass or Mediterranean tapeweed, is a seagrass species that is endemic to the Mediterranean Sea. It forms large underwater meadows that are an important part of the ecosystem. The fruit is free floating and known in Italy as "the olive of the sea" (l'oliva di mare). Balls of fibrous material from its foliage, known as egagropili or Neptune balls, wash up to nearby shorelines.
The Posidonia has a very high carbon absorption capacity, being able to soak up 15 times more carbon dioxide every year than a similar sized piece of the Amazon rainforest.
