Temporal and depth-associated changes in the structure, morphometry and production of near-pristine Zostera marina meadows in western Ireland

Highlights

• First baseline data of temporal changes in shoot and population dynamics, including biomass production, from western Ireland.

• Discernible temporal and site-specific differences in morphometry and population structure.

• Depth- acclimatization induced significant changes in the vegetative development.

• Latitudinal comparison of leaf production places Irish populations within global trend for temperate regions.

Abstract

The eelgrass Zostera marina is a dominant, subtidal meadow-forming seagrass in temperate regions in the northern hemisphere. Due to the numerous ecological services they provide, seagrass systems rank amongst the most valuable ecosystems worldwide but there is a lack of data regarding the structure and productivity of Irish seagrass populations. To address this gap, this investigation assessed temporal changes and depth acclimations of vegetative parameters, such as, shoot length and weight, shoot density, seagrass cover and below- and above-ground biomass, in three near-pristine subtidal Z. marina meadows in western Ireland. Most parameters revealed a marked temporal pattern, displaying clear unimodal responses, with peaks attained in July, intermediate values in April and November, and lowest values observed in January. Moreover, eelgrass cover and density decreased from 76.1 ± 6.5% in shallow meadows to 34 ± 4.5% at greater depths; inversely, other parameters such as shoot biomass or shoot length increased 2–3-fold with depth. Furthermore, annual leaf formation rates and above-ground biomass were estimated and compared to those of eelgrass populations from different latitudes (28°–66°) reported in the literature. Results suggest that the vegetative development of Irish populations corresponds to global data reported at different local and global scales of Z. marina populations inhabiting stable environments; our data serve as a first baseline for the assessment of potential future environmental impacts, including climate change and eutrophication.

Introduction

The study of keystone species is vital for biological management and conservation, in particular in view of currently observed impacts of global change, including anthropogenic disturbances and climatic environmental shifts (Thomas et al., 2004). Significant impacts at community and ecosystem level have been documented over the last few decades, so that there is a critical requirement for species monitoring and the preservation of key environmental indicators (Hoegh-Guldberg and Bruno, 2010). Non-polluted and undisturbed areas have been widely used as a baseline to monitor habitat disturbances and degradation; however, nowadays there is a lack of pristine environments, particularly in marine coastal ecosystems due to exposure to direct and indirect human pressures (Jackson et al., 2001; Knowlton and Jackson, 2008).

Seagrasses are angiosperms that complete their life cycle within marine environments and that are typically associated with sheltered and shallow habitats (Hemminga and Duarte, 2000). These macrophyte communities rank among the ecologically most valuable ecosystems worldwide due to the numerous services they provide, such as shoreline protection, habitat and nursery grounds, high oxygen and biomass productivity and carbon sequestration (e.g., Costanza et al., 1997; Fourqurean et al., 2012). However, they do not enjoy the international and social recognition as other charismatic ecosystems such as coral reefs or tropical forests (e.g. Nordlund et al., 2018). In temperate regions of the northern hemisphere, one of the main meadow-forming seagrasses is the eelgrass, Zostera marina Linnaeus. Displaying a broad distribution from subtropical regions to the Arctic Circle, between 27° and 70 °N, the species is adapted to a wide range of temperature regimes, from -1 °C in Arctic regions, to 30 °C in subtropical areas (Ibarra-Obando et al., 1997; Olesen et al., 2015; Ruiz et al., 2015). This adaptability renders Z. marina an exceptionally plastic character with regard to vegetative growth, life cycle and reproductive effort (i.e., Keddy, 1987; Meling-lópez and Ibarra-Obando, 1999).

Temperature and irradiance have been identified as the most relevant factors driving temporal variations of temperate seagrasses; they control metabolic processes such as photosynthesis and respiration (e.g., Zimmerman et al., 1995; Marsh et al., 1986; Sang and Park, 2005), but also affect the population structure, flowering and seed germination (i.e., Durako and Moffler, 1987; Diaz-Almela and Marbà, 2007; Moore et al., 1993; Stubler et al., 2017). Temperate eelgrasses typically exhibit marked seasonal growth, with optimal productivity rates observed during warmer periods with higher daylight hours during which leaf structures increase in biomass and size, allowing enhanced photosynthetic performance and subsequent storage of energy-rich compounds such as carbohydrates, mainly below-ground (Alcoverro et al., 2001). On the contrary, in colder and darker periods, seagrass shoot size decreases, thus reducing photosynthetic tissues, resulting in low metabolic rates and the utilisation of existing energy reserves (Bay et al., 1996; Alcoverro et al., 2001).

Irradiance is the main factor limiting seagrass vertical distribution, affecting shoot growth and productivity, and inducing changes at population level (e.g., Duarte, 1991; Olesen et al., 2002; Ralph et al., 2007). In temperate regions, light energy limitation of eelgrass growth is most pronounced for deep-adapted populations where irradiance allows seagrasses a marginally positive carbon budget on an annual basis (Dennison, 1987). At intermediate latitudes, eelgrass meadows at greater depth are generally characterized by low shoot densities, but greater shoot weights and wider leaves than shallow meadows, although peaks in shoot weight were also commonly observed at intermediate depths (i.e., Krause-Jensen et al., 2000; Olesen et al., 2017). Such an adaptive strategy allows plants to reduce self-shading and achieve higher light absorption, thus favouring a deeper colonization (Krause-Jensen et al., 2000).

Distributed in the middle of its latitudinal range (51°–55°N), Z. marina is the most dominant subtidal seagrass in Ireland which can colonize maximum depths of 10 m (NPWS, 2014; MERC, 2005). However, only few studies have, even peripherally, addressed Irish eelgrass population ecology (Dale et al., 2007; Jones and Unsworth, 2016; Wilkes et al., 2017). Ireland’s climate is defined as a temperate oceanic climate, characterized by clearly defined climatic periods with a lack of extreme cold or warm temperatures (https://www.met.ie; Peel et al., 2007). Due to their relative inaccessibility and the generally low anthropogenic impacts in remote coastal areas in western Ireland, large undisturbed seagrass meadows may have persisted until the present day.

We hypothesize that Irish eelgrasses may show a discernible temporal pattern regarding shoot growth and population dynamics as Ireland is characterized by distinct, environmentally defined, seasons. Secondly, we propose that low-light conditions at greater depth induce changes in vegetative development. In addition, we propose that annual leaf formation rates and above-ground biomass production in Irish populations is related to local surface water temperatures and follow large-scale longitudinal trends. Therefore, the objectives of this study were to characterize the temporal changes of plant descriptors at shoot and population level in three meadows in populations from western Ireland. Adaptations to depth-related environmental conditions were assessed by comparing temporal performance of plants from different depths. Finally, we evaluated the annual leaf formation rate and above-ground biomass across their geographical distribution range (27˚ – 66 °N) in relation to in situ summer and annual seawater surface temperatures (SST).