Understanding the sexual recruitment of one of the oldest and largest organisms on Earth, the seagrass Posidonia oceanica

Abstract

The seagrass Posidonia oceanica is considered one of the oldest and largest living organisms on Earth. Notwithstanding, given the difficulty of monitoring its fruits and seeds in the field, the development of P. oceanica during its sexual recruitment is not completely understood. We studied the stages of development of P. oceanica seeds from their dispersion in the fruit interior to their settlement in sediment through histological, ultrastructural and mesocosm experiments. P. oceanica sexual recruitment can be divided into three main stages that focus on maximising photosynthesis and anchoring the seedlings to the sediment. In the first stage (fruit dispersion), seeds perform photosynthesis while being transported inside the fruit along the sea surface. In the second stage (seed adhesion), seeds develop adhesive microscopic hairs that cover the primary and secondary roots and favour seed adhesion to the substrate. In the last stage (seedling anchorage), roots attach the seedlings to the substrate by orienting them towards the direction of light to maximise photosynthesis. The adaptations observed in P. oceanica are similar to those in other seagrasses with non-dormant seeds and fruits with membranous pericarps, such as Thalassia sp. and Enhalus sp. These common strategies suggest a convergent evolution in such seagrasses in terms of sexual recruitment. Understanding the sexual recruitment of habitat-forming species such as seagrasses is necessary to adequately manage the ecosystems that they inhabit.

Fig 1. Newly released and 1-week-old seeds of P. oceanica.

(A) Newly released seeds inside a fruit and (B) 1-week-old seeds of Posidonia oceanica. FP, fruit pericarp; NRS, newly released seeds; WS, 1-week-old seeds; H, adhesive hairs; S, seed; R1, primary root; Rh, rhizome; L, leaves.

Fig 2. Details of the histology, ultrastructure and morphology of the fruit pericarp and 1-week-old seeds of Posidonia oceanica.

Images show (A) the histological fruit pericarp sections and (B and C) the ultrastructure of the adhesive basal hairs of a 1-week-old seed. Green arrows indicate chloroplasts, while blue arrows denote air lacunae. Ed, epidermis; Hd, hypodermis; M, mesophyll; H, adhesive hairs; S, seed.

Fig 3. Influence of light on the sexual recruitment of P. oceanica.

The graphs show the results obtained in the experiments performed to test the influence of light on the sexual recruitment of Posidonia oceanica (mean±SE; n = 5): (A) light transmitted by the fruit pericarps in a gradient of light irradiance; (B) RLCs; (C) light-adapted yields of the fruit pericarp and seeds; (D) GPP; (E) NPP; and (F) respiration obtained in newly released (NRS) and 1-week-old seeds (WS) at a light intensity of 10 μE · m^-2 · s^-1. Lines indicate significant regressions (p< 0.01) in the fruit pericarps (black lines; R² = 0.98), newly released seeds (dotted black lines; R² = 0.96) and 1-week-old seeds (dotted grey lines; R² = 0.97). Letters indicate significant pairwise differences between the treatments.

Fig 4. Root hair ultrastructure of P. oceanica.

Images obtained by scanning electron microscopy of the root hairs of the Posidonia oceanica seedlings grown in different types of sediment treatments: (A) root hairs adhered by their basal extreme in the pebble treatment, (B) root hairs surrounding grains of sand in the sand treatment, (C) root hairs that interwove a fibre in the fibreglass treatment, (D) the branched edges of root hairs, (E) the basal extreme of a root hair anchored to the pebble treatment and (F) the microvillus of the lateral surface of root hairs.

Fig 5. Schematic representation of the three sexual recruitment stages of P. oceanica, including dispersion and settlement.