For decades, Zostera marina (Linneo) and Zostera noltei (Hornemann) have faced a severe decline across their range (Orth et al. 2006, Waycott et al. 2009, Short et al. 2011). Although the recovery of degraded ecosystems without direct restoration intervention is rare, in recent years, certain coastal areas have displayed considerable resilience (Lotze et al. 2006, Dolch et al. 2013, Folmer et al. 2016). Unfortunately, little attention has been given in the scientific literature to resilient ecosystems, and resilience drivers remain poorly understood (Macreadie et al. 2014, Yaakub et al. 2014, Hughes et al. 2016).

To halt degradation and promote recovery, management requires a change in emphasis to enhance seagrass ecosystem resilience (Unsworth et al. 2015). In addition to the ability to recover that has been demonstrated by small fast-growing seagrass species such as Z. marina and Z. noltei (Davis et al. 2016), seagrass meadows also need to possess traits of resistance in order to remain resilient to drivers of ecosystem change (Bergmann et al. 2010).

Unsworth et al. (2015) classify seagrass resilience traits into biological features of seagrasses (e.g. leaf width and length, density and tolerance to abiotic features), biological features of supporting ecosystems (e.g. species assemblages) and biophysical environment (e.g. water quality). Thus, large, dense, non-fragmented meadows in healthy environments and with good trophic interactions might enhance the resilience of seagrasses (Ehlers et al. 2008).

The Bay of Santander is the largest estuary in northern Spain (Bay of Biscay). This tidal ecosystem shelters perennial seagrass meadows of Z. noltei in the intertidal and Z. marina in the low tidal and shallow subtidal zones. Recently, Calleja et al. (2017) reported a decline in Z. noltei that occurred in the Bay of Santander between 1984 and the early 2000s. During the decline they observed that one of the meadows (La Barquería) maintained large populations of seagrasses and showed uninterrupted growth. They concluded that the resistance of this meadow to the changes that had affected seagrass meadows in the Bay of Santander in past decades could be a reflection of the resilience.

Where seagrasses have traditionally existed, the combination of maturity and changing environmental conditions could be enabling a healthier and more resilient community (Calleja et al. 2017). The meadow is subjected to episodic storm events in the river basin that result in severely changing conditions arising from large amounts of suspended solids reaching the estuary from the eroded watershed. Consequently, seagrasses in this area have adapted to tolerating periodic phases of turbidity and severe changes in temperature, light, salinity and nutrient concentrations.

The objective of this work was to study the resilient meadow of La Barquería at the precise moment when the population of seagrasses was decreasing in the Bay of Santander (in the year 2000). Based on Unsworth et al. 2015, the meadow was characterized by analysing a selection of resilience biological features, which included habitat characteristics, trait variability in shoot density, aboveground biomass, leaf length and width, and benthic assemblages for Zostera marina and Zostera noltei beds along seasonal and spatial gradients.

The present work analyses a meadow that maintained large populations of Zostera marina and Zostera noltei during the decline observed in the Bay of Santander from 1984 to the early 2000s. The significance of this kind of resilient meadow resides in its implications for management. These areas may function as seed sources and allow the recovery of lost areas (Calleja et al. 2017). When considering seagrass resistance and recovery, it is generally agreed that the greater the trait variability, the more likely the system is to survive periods of stress (Maxwell et al. 2014). A main aspect of such studies is to understand how local factors are compromising and, in some cases, contributing to the resilience of seagrass ecosystems (Unsworth et al. 2015). Although this study does not focus on analysing the causes, there is evidence in the literature suggesting that exposure to certain environmental stresses may enable individuals or communities to adapt to drivers and improve their resistance (Maxwell et al. 2014, Calleja et al. 2017).

In contrast with the findings of the literature on other Atlantic estuaries (e.g. Cochón et al. 2005, Martin et al. 2010, Garmendia et al. 2017), in the Bay of Santander the decline was followed by a fast recovery characterized by patches of vegetation alternating in space and time. Today, Z. marina and Z. noltei occupy most of the shallow tidal flats in the Bay of Santander (Ondiviela et al. 2015), and the high recovery rate observed suggests that resilient meadows played an important role in this process. At the local scale, recolonization processes can be driven by resilient meadows able to absorb disturbances and adapt to change during acute decline periods (Holling 1973).

To better understand resilient meadows, La Barquería was characterized by analysing plant traits (biomass, density, leaf width and length) and benthic assemblages along two factors of variation: seasonality and freshwater influence. In La Barquería Z. marina and Z. noltei are perennial. Both species display a similar and noticeable seasonal growth pattern related to the summer peaks in the photosynthetically active radiation and the sea surface temperature (Lee et al. 2007, Ondiviela et al. 2014; Fig. 7). They also show a unimodal biomass pattern, which is a common feature of seagrass meadows found in temperate shallow waters (Olesen and Sand-Jensen 1994, Laugier et al. 1999, Lee et al. 2007). During the spring, new leaves are produced and grow in both length and width. During the summer, when there is plenty of activity, these two seagrass species reach their annual maximum biomass. Beginning in the fall (e.g. September), the plants achieve their maximum length and lose mature leaves, which are the longest and have the highest biomass. Likewise, a generic relationship is found between the biomass and shoot density of the beds and the spatial gradient along the river discharge, which increases upstream of the river, through the sites with high freshwater influence.

For Z. marina, the observed mean aboveground biomass and shoot density resemble those of other temperate and well conserved meadows in estuaries of southern Spain (220-402 shoots m^–2; 8.4-90 g DW m^–2; Rueda et al. 2008) and the Atlantic coast of Canada (460-1046 shoots m^–2; 20-120 g DW m^–2; Wong et al. 2013). The observed values for Z. noltei also agree well with data from comparable climatic conditions in the southwestern Iberian Peninsula (2000-10000 shoots m^–2; 6-13 cm leaf length; 0.09-0.17 cm leaf wide; Peralta 2000, Peralta et al. 2000); and the Arcachon Bay in France (40-110 g DW m^–2; 4000-22000 shoots m^–2; Auby and Labourgm 1996).

Invertebrate assemblages frequently reflect habitat variability. Physical factors typically determine macro-scale (e.g. kilometre scale) patterns of assemblages, while food distribution, habitat structure, biotic interactions and reproductive behaviour cause micro-scale (e.g. metre scale) heterogeneity (Baeta et al. 2009, Cunha et al. 2013, Materatski et al. 2016). In La Barquería relationships between environmental gradients, aboveground biomass and benthic assemblages appear to be helping define the composition of the meadow. These factors might be related to the abundance and distribution of Hydrobia ulvae in zones with a high freshwater influence and the associations between Rissoa parva and Z. marina and between Bittium reticulatum and Z. noltei in areas with a high marine influence. Seagrasses are frequently characterized by the abundance of certain faunal groups (Cardoso et al. 2008, Virnsten et al. 1984). In La Barquería grazers dominate sites characterized by low hydrodynamics, stable sediment and relatively high tidal levels. The consequence is a spatial gradient along the axial channel of the river, which is highly evident in the Z. noltei bed, with fauna abundance declining and diversity and richness increasing towards the areas where the marine influence is higher. By contrast, seasonal changes caused by temperature and irradiance do not highly affect fauna assemblages.

The present study characterizes the resilient meadow of La Barquería at the precise moment when the population of Zostera marina and Zostera noltei was decreasing in the Bay of Santander (from 1984 to the early 2000s). A number of resilient parameters related to plant traits (biomass, density, leaf length and width) and benthic assemblages along two factors of variation (seasonality and freshwater influence) were analysed. In La Barquería, Z. marina and Z. noltei beds display traits of resistance for remaining resilient. The two species show high variability in these traits, making evident that the greater the trait variability, the more likely the system is to survive periods of stress. The biomass, density, morphological traits and benthic assemblages vary as a function of seasonal and spatial gradients. This variation is probably related to the summer peaks in the photosynthetically active radiation, the sea surface temperature and the freshwater influence along the discharge of the Miera River. A small number of species dominate the structure and composition of the benthic macrofauna. The gradients along the river discharge determine the abundance and distribution of Hydrobia ulvae in zones with a high freshwater influence and the associations between Rissoa parva and Z. marina and between Bittium reticulatum and Z. noltei in zones with a high marine influence. This work provides the first seagrass data in Cantabria and may constitute a baseline study for the Bay of Biscay.