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Sediment Characteristics Determine the Flowering Effort of Zostera Noltei Meadows Inhabiting a Human-Dominated Lagoon

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Sediment Characteristics Determine the Flowering Effort of Zostera Noltei Meadows Inhabiting a Human-Dominated Lagoon plants Article Sediment Characteristics Determine the Flowering Effort of Zostera noltei Meadows Inhabiting a Human-Dominated Lagoon Laura Guerrero-Meseguer 1,2,* , Puri Veiga 1,2, Leandro Sampaio 1,2 and Marcos Rubal 1,2 1 Interdisciplinary Centre of Marine and Environmental Research (CIIMAR) of the University of Porto, Novo Edifício do Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, 4450-208 Matosinhos, Portugal; [email protected] (P.V.); [email protected] (L.S.); [email protected] (M.R.) 2 Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre s/n, 4169-007 Porto, Portugal * Correspondence: [email protected] Abstract: Recent studies have shown increasing Zostera noltei meadows in areas modified by anthro- pogenic activities. However, it is not entirely clear whether this trend of expansion could be linked to a greater reproductive effort in the species. Anthropogenic stressors can induce the reproductive effort of seagrass meadows as a response to stress, but other variables, such as seagrass biometrics or environmental factors, can also influence their sexual reproduction. To increase the knowledge regarding this issue, we monitored the flowering effort, seagrass biometrics and abiotic parameters of three Z. noltei meadows in an area that has been highly modified by anthropogenic activities during the past decades. Results showed that silt and clay content in the sediment (strongly correlated with Citation: Guerrero-Meseguer, L.; organic matter) and seagrass vertical shoot density explained 54% of the variability in the flowering Veiga, P.; Sampaio, L.; Rubal, M. effort of the meadows. This study suggests that stress-induced flowering of Z. noltei may occur under Sediment Characteristics Determine determinate environmental conditions, such as silty environments with organic enrichment. the Flowering Effort of Zostera noltei Meadows Inhabiting a Human- Keywords: seagrass; sexual reproduction; anthropogenic stressors; sediment; organic matter Dominated Lagoon. Plants 2021, 10, 1387. https://doi.org/10.3390/ plants10071387 1. Introduction Academic Editor: Stefano Accoroni Seagrasses establish key ecosystems around the world, playing important ecological roles [1]. Among others, seagrass meadows preserve the coastal geomorphology, are Received: 4 May 2021 responsible for seawater quality and clarity, and provide shelter, nursery and feeding Accepted: 5 July 2021 Published: 6 July 2021 areas for numerous marine organisms [2–4]. Although seagrasses cover only 0.1% of the world’s ocean floor, they significantly contribute to its primary production and carbon Publisher’s Note: MDPI stays neutral sequestration [5–9], but have been threatened by anthropogenic stressors over the past with regard to jurisdictional claims in decades [10]. published maps and institutional affil- Seagrasses can inhabit intertidal and subtidal areas of estuaries and lagoons [10]. In iations. recent decades, the influence of human activities such as aquaculture, dredging, wastew- ater or stormwater runoffs, shellfish harvesting and boat transit have strongly modified these ecosystems’ functioning [11,12]. The above-mentioned anthropogenic activities can cause, among others, mechanical impacts across the seagrass meadows and changes in their sediment composition [13–15]. Nevertheless, recent studies suggest that some sea- Copyright: © 2021 by the authors. Zostera Licensee MDPI, Basel, Switzerland. grass species, especially of the genus , are currently adapting to human-modified This article is an open access article environments [16–22]. distributed under the terms and Zostera noltei Hornemann is one of the seagrass species that best tolerates human- conditions of the Creative Commons dominated environments. This seagrass shows characteristics of opportunistic species, Attribution (CC BY) license (https:// displaying a high shoot turnover and forming seed banks in the sediments, which allow creativecommons.org/licenses/by/ it to quickly recover after unfavorable periods or anthropogenic disturbances [1,23]. In 4.0/). addition, the species inhabits a wide range of salinities (7–35 psu) [24,25], can tolerate Plants 2021, 10, 1387. https://doi.org/10.3390/plants10071387 https://www.mdpi.com/journal/plants Plants 2021, 10, 1387 2 of 13 elevated seawater temperatures (above 37 ◦C) [26] and adapts to high light exposure conditions during low tide [27]. Thus, Z. noltei is suited to intertidal areas of estuaries and lagoons, such as Ria de Aveiro, which are also environments dominated by several human activities [16,20]. Numerous studies have shown that there is a positive trend in this seagrass expansion amidst environments dominated by human activities during recent decades (i.e., shellfish harvesting and dredging) [16,20]. Moreover, the flowering effort of Z. noltei can increase under the influence of certain anthropogenic perturbations such as mechanical, sedimentary and hydrodynamic impacts [28–30]. However, the reproductive capacity of Z. noltei in human-dominated areas where the species is expanding has not yet been evaluated. Although seagrass expansion can be maintained only by asexual reproduction of its own rhizomes, sexual reproduction sustains the long-term survival of the species when vegetative growth is limited [31–33]. In addition, sexual reproduction on seagrasses provides genetic diversity, which is essential for clonal organisms since it allows them to improve their survival when facing upcoming stressors [34,35]. Thus, understanding the sexual reproduction of Z. noltei in human-dominated environments could provide some insight about the expansion drift of this species. Modifications in abiotic parameters (i.e., temperature, salinity and light intensity) can influence the timing and intensity of the flowering in Zostera species, leading to high spatial variability in their reproductive effort [36–38]. At high latitudes, the flowering of Z. noltei starts in the hottest spring months and ends when the temperatures start to drop, by the end of autumn [36,39]. Although the mechanisms that control sexual reproduction in this seagrass are not yet fully understood, it is known that its flowering effort can vary under different sediment types, colonization stages and vegetative growth capacity [28,29,40,41]. Therefore, evaluating the flowering of Z. noltei in an environment with great spatial variability and subject to multiple and simultaneous anthropogenic stressors, such as Ria de Aveiro, can help us forecast the future of impacted meadows and understand which factors could influence the stress-induced flowering response of this seagrass. The aim of this study was to determine if seagrass biometrics and environmental factors could influence the flowering of human-dominated Z. noltei meadows. To test this, the flowering effort, seagrass biometrics and abiotic parameters of three Z. noltei meadows inhabiting an area subjected to several anthropogenic activities (dredging, oyster culture, stormwater runoffs and bait digging) were measured during the period of sexual reproduction. The relationship between the flowering effort of the species and biometric and abiotic parameters was also analyzed. 2. Material and Methods 2.1. Study Area The present study was done in the Mira channel of the Ria de Aveiro lagoon (Aveiro, Portugal; Figure1A). This channel is an elongated and shallow arm, 25 km long, that runs south-southwest, parallel to the coastline (Figure1A). During floods, only about 20% of the tidal prism is diverted to this channel, while a continuous freshwater supply is received in the upper part through a small system of lagoons and streams. This creates a salinity gradient during high tides, with very low salinities in the most internal areas (0−5 psu), high values at the mouth (25−36 psu) and highly variable salinity ranges in the middle section of the channel [42], where the study was conducted. The Ria de Aveiro lagoon has been highly modified by human activities over the past decades, resulting in a spatial mosaic of different environmental conditions, especially regarding sediment composition. This lagoon is frequently subjected to dredging to prevent siltation and to maintain hydrodynamics of its channels, widely used for navigation and recreational purposes [43]. Dredging activities have increased the penetration of the tidal wave, enhancing turbidity and causing resuspension of coarse sandy sediments from the deepest areas of the lagoon and their deposition to the tidal flats nearby [44]. Other common anthropogenic pressures in Ria de Aveiro are fishing and related activities Plants 2021, 10, 1387 3 of 13 such as bait digging, shellfish harvesting or the use of motor boating, which have a high potential of disturbing the sediment [14]. The erosion of the sediments promoted by these anthropogenic activities is causing the loss of finer sediments, nutrients and organic matter content in the Z. noltei meadows of the lagoon, producing negative impacts in their development [45]. Figure 1. Study area (Ria de Aveiro, Center of Portugal) (A) and location of the three Z. noltei meadows in the Mira Channel (B). The dark area in (B) indicates the location of the oyster farming, while the blue arrows indicate the position of the storm drain outlets. The white, grey and black spots of (B) show the location of each Z. noltei meadow. (C) shows the storm drain outlet and runoff of the Meadow C. (D) displays the oyster farm trestles and farming activities in Meadow B. Apart from the above-mentioned anthropogenic
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